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The Multifaceted COVID-19: CT Aspects of Its Atypical Pulmonary and Abdominal Manifestations and Complications in Adults and Children. A Pictorial Review

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Our daily experience in a COVID hospital has allowed us to learn about this disease in many of its changing and unusual aspects. Some of these uncommon manifestations, however, appeared more frequently than others, giving shape to a multifaceted COVID-19 disease. This pictorial review has the aim to describe the radiological aspects of atypical presentations and of some complications of COVID-19 disease in adults and children and provide a simple guide for radiologists to become familiar with the multiform aspects of this disease.
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microorganisms
Review
The Multifaceted COVID-19: CT Aspects of Its Atypical
Pulmonary and Abdominal Manifestations and Complications
in Adults and Children. A Pictorial Review
Chiara Morelli 1, *, Mariantonietta Francavilla 2, Amato Antonio Stabile Ianora 1, Monica Cozzolino 1,
Alessandra Gualano 1, Giandomenico Stellacci 2, Antonello Sacco 1, Filomenamila Lorusso 1, Pasquale Pedote 1,
Michele De Ceglie 1and Arnaldo Scardapane 1


Citation: Morelli, C.; Francavilla, M.;
Stabile Ianora, A.A.; Cozzolino, M.;
Gualano, A.; Stellacci, G.; Sacco, A.;
Lorusso, F.; Pedote, P.; De Ceglie, M.;
et al. The Multifaceted COVID-19: CT
Aspects of Its Atypical Pulmonary
and Abdominal Manifestations and
Complications in Adults and
Children. A Pictorial Review.
Microorganisms 2021,9, 2037. https://
doi.org/10.3390/microorganisms9102037
Academic Editor:
Sofia Costa-de-Oliveira
Received: 31 July 2021
Accepted: 23 September 2021
Published: 26 September 2021
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Attribution (CC BY) license (https://
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4.0/).
1
Interdisciplinary Department of Medicine, Section of Diagnostic Imaging, University of Bari Medical School,
70124 Bari, Italy; amatoantonio.stabileianora@uniba.it (A.A.S.I.); monicacoz@hotmail.it (M.C.);
alegualano@gmail.com (A.G.); sacccoanto@gmail.com (A.S.); milalorusso@yahoo.it (F.L.);
pedoterx@gmail.com (P.P.); micheledeceglie@libero.it (M.D.C.); arnaldo.scardapane@gmail.com (A.S.)
2Unit of Pediatric Imaging, Giovanni XXIII Hospital, 70126 Bari, Italy; marianto_fra@hotmail.it (M.F.);
gstellacci@icloud.com (G.S.)
*Correspondence: dottchiaramorelli@gmail.com
Abstract:
Our daily experience in a COVID hospital has allowed us to learn about this disease in
many of its changing and unusual aspects. Some of these uncommon manifestations, however,
appeared more frequently than others, giving shape to a multifaceted COVID-19 disease. This
pictorial review has the aim to describe the radiological aspects of atypical presentations and of
some complications of COVID-19 disease in adults and children and provide a simple guide for
radiologists to become familiar with the multiform aspects of this disease.
Keywords: COVID-19; atypical manifestation; CT; adult; children; pulmonary; abdominal
1. Introduction
On 31 December 2019, the Chinese health authority announced an outbreak of pneu-
monia cases of unknown etiology in Wuhan (Hubei, China). On 9 January 2020, the China
Center for Disease Control and Prevention (CDC, Beijiing CHN) identified a new coro-
navirus (temporarily named 2019-nCoV) as the etiological cause of this disease. They
later confirmed the inter-human transmission of the virus. On 11 February, the World
Health Organization (WHO, Geneva CH) announced that pneumonia caused by 2019-nCoV
was called COVID-19 (Corona Virus Disease 19). The Coronavirus Study Group of the
International Committee on Taxonomy of Viruses has classified the virus under the name
of SARS-CoV-2, associating it with the coronaviruses that cause severe acute respiratory
syndrome (SARS-CoVs, severe acute respiratory syndrome coronaviruses). On 11 March
2020, the WHO, after assessing the severity levels and global spread of the SARS-CoV-2
infection, declared the COVID-19 pandemic. There are 190,770,507 confirmed cases in the
world since the beginning of the pandemic and 4,095,924 deaths [1].
While Reverse Transcriptase Polymerase Chain Reaction (RT PCR) remains the diag-
nostic gold standard of infection, computed tomography (CT) has been shown to have
a fundamental role in diagnosis, especially in those patients with false negative RT PCR
results, with a sensitivity of approximately 98%. The CT examination allows us to mon-
itor the progression of the disease and evaluate the multi-organ involvement. Thanks
to CT, we have learned to recognize the typical pulmonary presentation (which we will
describe below). Nevertheless, both the literature data and our direct experience require
us to keep in mind that this pathology can often show itself “in disguise”, giving atypical,
non-classical, unexpected and complicated manifestations: it is necessary to know them in
order to avoid misunderstandings.
Microorganisms 2021,9, 2037. https://doi.org/10.3390/microorganisms9102037 https://www.mdpi.com/journal/microorganisms
Microorganisms 2021,9, 2037 2 of 19
Typical SARS-CoV-2 pneumonia is well known and it is characterized by bilateral,
multilobar, peripheral, subpleural ground glass opacity [
2
] (Figure 1). In the most ad-
vanced stages of the disease, however, parenchymal consolidations, and thickening of the
interlobular septa with crazy paving patterns will be frequently visible [3].
Microorganisms 2021, 9, 2037 2 of 21
us to keep in mind that this pathology can often show itself “in disguise”, giving atypical,
non-classical, unexpected and complicated manifestations: it is necessary to know them
in order to avoid misunderstandings.
Typical SARS-CoV-2 pneumonia is well known and it is characterized by bilateral,
multilobar, peripheral, subpleural ground glass opacity [2] (Figure 1). In the most
advanced stages of the disease, however, parenchymal consolidations, and thickening of
the interlobular septa with crazy paving patterns will be frequently visible [3].
Atypical manifestations may affect both adult and pediatric patients with pulmonary
and extra-pulmonary involvement.
Figure 1. Computed tomography (CT) axial image of ground glass opacity. A hospitalized COVID-
19 patient with fever and dyspnea. The axial CT image shows bilateral ground glass opacities with
peripheral subpleural disposition in the right lung and tending to confluence in the left lung.
Spontaneous pneumomediastinum is associated.
2. Adult “Atypical” and “Complicated” Pulmonary COVID-19
Lymphadenopathy, pleural effusion, pericardial effusion, bronchiectasis, halo sign
and reverse halo sign, cavitation and some complications, such as spontaneous
pneumothorax and pneumomediastinum, are reported as either pulmonary unusual
manifestations or atypical complications of COVID-19 [4–7]. As we will clarify below, if
lymphadenopathies are more often found in acute phase of the disease, the pleural
effusion is frequently identified in the advanced stages. Furthermore, while
lymphadenopathies are linked to patients with stronger immune response, pericardial
effusion is associated with the worst COVID-19 cases, in which heart damage coexists.
2.1. Lymphadenopathy
With the term “lymphadenopathy” we refer to mediastinal lymph nodes >10 mm and
hilar lymph nodes >3 mm in short axis diameter. As already reported by Li et al. [8], and
by Grassi et al. [9], lymphadenopathies are part of the acute COVID-19 manifestations
even if they do not represent a specific and characteristic sign (Figure 2). Xiao Li et al. [10]
reported that hilar and mediastinal lymph node enlargement was observed in 43.51% of
patients with COVID-19 pneumonia. Their study suggested that enlarged hilar and
mediastinal lymph nodes are associated with immune response and that patients with
COVID-19 pneumonia have stronger immune response especially in moderate and severe
conditions.
Figure 1.
Computed tomography (CT) axial image of ground glass opacity. A hospitalized COVID-
19 patient with fever and dyspnea. The axial CT image shows bilateral ground glass opacities
with peripheral subpleural disposition in the right lung and tending to confluence in the left lung.
Spontaneous pneumomediastinum is associated.
Atypical manifestations may affect both adult and pediatric patients with pulmonary
and extra-pulmonary involvement.
2. Adult “Atypical” and “Complicated” Pulmonary COVID-19
Lymphadenopathy, pleural effusion, pericardial effusion, bronchiectasis, halo sign and
reverse halo sign, cavitation and some complications, such as spontaneous pneumothorax
and pneumomediastinum, are reported as either pulmonary unusual manifestations or
atypical complications of COVID-19 [
4
7
]. As we will clarify below, if lymphadenopathies
are more often found in acute phase of the disease, the pleural effusion is frequently
identified in the advanced stages. Furthermore, while lymphadenopathies are linked to
patients with stronger immune response, pericardial effusion is associated with the worst
COVID-19 cases, in which heart damage coexists.
2.1. Lymphadenopathy
With the term “lymphadenopathy” we refer to mediastinal lymph nodes >10 mm and
hilar lymph nodes >3 mm in short axis diameter. As already reported by Li et al. [
8
], and by
Grassi et al. [
9
], lymphadenopathies are part of the acute COVID-19 manifestations even if
they do not represent a specific and characteristic sign (Figure 2). Xiao Li et al. [
10
] reported
that hilar and mediastinal lymph node enlargement was observed in 43.51% of patients
with COVID-19 pneumonia. Their study suggested that enlarged hilar and mediastinal
lymph nodes are associated with immune response and that patients with COVID-19
pneumonia have stronger immune response especially in moderate and
severe conditions.
Microorganisms 2021,9, 2037 3 of 19
Microorganisms 2021, 9, 2037 3 of 21
Figure 2. CT axial images of mediastinal lymphadenopathies. Enlarged lymph nodes with short axis of 13.4 mm and 16.1
mm are evident in the lower pre-tracheal space (A) and in the aorto-pulmonary window (B), respectively.
2.2. Pleural Effusion
Pleural effusion is rarely associated with COVID-19. We often find it in the most
critically ill patients and in the most advanced stages of the disease (Figure 3). Zhou [11]
et al. described pleural effusion in 3.2% of COVID-19 patients while Grassi et al. [9]
observed it in 14.3% of cases. Darwish et al. [12]
found that during the first week of
infection pleural effusion occurs only in 13.6% of patients. Xiao li et al. [10], in regard to
pleural effusion, reported a frequency of 14.3% and concluded that it was not significantly
associated with COVID-19 pneumonia.
Figure 3. A 58-year-old female patient with worsening respiratory function on the 10th day of hospitalization evaluated
with CT. Sagittal (A) and axial (B) images show posterior pleural effusion greater on the left side.
2.3. Pericardial Effusion
Pericardial effusion can be defined as the presence of more than 50 mL of liquid
between the pericardial sheets. As already mentioned for the pleural effusion it is not
characteristic of the COVID-19 thoracic involvement. In fact, it was observed by Li et al.
[8] in 4.8% of cases. However, in this study, it is also described as a manifestation
associated with the most compromised patients (Figure 4).
A B
A B
Figure 2.
CT axial images of mediastinal lymphadenopathies. Enlarged lymph nodes with short axis of 13.4 mm and
16.1 mm are evident in the lower pre-tracheal space (A) and in the aorto-pulmonary window (B), respectively.
2.2. Pleural Effusion
Pleural effusion is rarely associated with COVID-19. We often find it in the most criti-
cally ill patients and in the most advanced stages of the disease (Figure 3).
Zhou [11] et al.
described pleural effusion in 3.2% of COVID-19 patients while Grassi et al. [
9
] observed it
in 14.3% of cases. Darwish et al. [
12
] found that during the first week of infection pleural
effusion occurs only in 13.6% of patients. Xiao li et al. [
10
], in regard to pleural effusion,
reported a frequency of 14.3% and concluded that it was not significantly associated with
COVID-19 pneumonia.
Microorganisms 2021, 9, 2037 3 of 21
Figure 2. CT axial images of mediastinal lymphadenopathies. Enlarged lymph nodes with short axis of 13.4 mm and 16.1
mm are evident in the lower pre-tracheal space (A) and in the aorto-pulmonary window (B), respectively.
2.2. Pleural Effusion
Pleural effusion is rarely associated with COVID-19. We often find it in the most
critically ill patients and in the most advanced stages of the disease (Figure 3). Zhou [11]
et al. described pleural effusion in 3.2% of COVID-19 patients while Grassi et al. [9]
observed it in 14.3% of cases. Darwish et al. [12]
found that during the first week of
infection pleural effusion occurs only in 13.6% of patients. Xiao li et al. [10], in regard to
pleural effusion, reported a frequency of 14.3% and concluded that it was not significantly
associated with COVID-19 pneumonia.
Figure 3. A 58-year-old female patient with worsening respiratory function on the 10th day of hospitalization evaluated
with CT. Sagittal (A) and axial (B) images show posterior pleural effusion greater on the left side.
2.3. Pericardial Effusion
Pericardial effusion can be defined as the presence of more than 50 mL of liquid
between the pericardial sheets. As already mentioned for the pleural effusion it is not
characteristic of the COVID-19 thoracic involvement. In fact, it was observed by Li et al.
[8] in 4.8% of cases. However, in this study, it is also described as a manifestation
associated with the most compromised patients (Figure 4).
A B
A B
Figure 3.
A 58-year-old female patient with worsening respiratory function on the 10th day of hospitalization evaluated
with CT. Sagittal (A) and axial (B) images show posterior pleural effusion greater on the left side.
2.3. Pericardial Effusion
Pericardial effusion can be defined as the presence of more than 50 mL of liquid
between the pericardial sheets. As already mentioned for the pleural effusion it is not
characteristic of the COVID-19 thoracic involvement. In fact, it was observed by Li et al. [
8
]
Microorganisms 2021,9, 2037 4 of 19
in 4.8% of cases. However, in this study, it is also described as a manifestation associated
with the most compromised patients (Figure 4).
Microorganisms 2021, 9, 2037 4 of 21
Figure 4. Pericardial effusion on CT, sagittal (A) and axial (B) images, in two patients admitted to intensive care unit. In
image B, bilateral pleural effusion is also noted.
Ali Sabri et al. [13] found a 7.9% frequency of pericardial effusion. Furthermore, from
their analysis, it emerged that pericardial effusion could be considered an important factor
for admission to intensive care unit (ICU), as it could be an indicator of myocarditis or
cardiomyopathy caused by COVID-19, but they did not confirm this hypothesis with
echocardiography.
Grassi et al. [9] describe pericardial effusion in 16.7% of patients, proposing a relation
with heart damage; Shi et al. [14] associated it with a higher risk of in-hospital mortality.
2.4. Bronchiectasis
Although bronchiectasis is not a typical COVID-19 manifestation (as noticed by
Salehi et al. [15]), it has been reported with a very high frequency (41.3%) by Auger et al.
[16]. They hypothesize that their result is probably due to the particularly compromised
clinical status of the patients included in the study. Devie et al. [17]
detected
bronchiectases and traction bronchiectases in 25.3% of cases, and concluded that these
cases were significantly more frequent in the most severe group of patients.
2.5. Halo Sign and Reverse Halo Sign
Halo sign consists of a shaded area of increased parenchymal density surrounded by
peripheral ground glass changes. It was studied by Wu and Chen et al. [18],
who
discovered it in 18/130 COVID-19 patients (13%), considering it as an unusual feature
associated with the initial phase of the disease. The reverse halo sign can be defined as a
clearly rounded area of “ground glass-like” increased parenchymal density,
circumscribed by a consolidation ring (Figure 5). It likely represents the disease
progression towards consolidation as described by Bernheim et al. [19],
who detected it in
4% of the patients studied at 6–12 days of infection.
A B
Figure 4.
Pericardial effusion on CT, sagittal (
A
) and axial (
B
) images, in two patients admitted to intensive care unit. In
image B, bilateral pleural effusion is also noted.
Ali Sabri et al. [
13
] found a 7.9% frequency of pericardial effusion. Furthermore,
from their analysis, it emerged that pericardial effusion could be considered an important
factor for admission to intensive care unit (ICU), as it could be an indicator of myocarditis
or cardiomyopathy caused by COVID-19, but they did not confirm this hypothesis with
echocardiography.
Grassi et al. [
9
] describe pericardial effusion in 16.7% of patients, proposing a relation
with heart damage; Shi et al. [14] associated it with a higher risk of in-hospital mortality.
2.4. Bronchiectasis
Although bronchiectasis is not a typical COVID-19 manifestation (as noticed by
Salehi et al. [15])
, it has been reported with a very high frequency (41.3%) by
Auger et al. [16]
.
They hypothesize that their result is probably due to the particularly compromised clinical
status of the patients included in the study. Devie et al. [
17
] detected bronchiectases and
traction bronchiectases in 25.3% of cases, and concluded that these cases were significantly
more frequent in the most severe group of patients.
2.5. Halo Sign and Reverse Halo Sign
Halo sign consists of a shaded area of increased parenchymal density surrounded
by peripheral ground glass changes. It was studied by Wu and Chen et al. [
18
], who
discovered it in 18/130 COVID-19 patients (13%), considering it as an unusual feature
associated with the initial phase of the disease. The reverse halo sign can be defined as a
clearly rounded area of “ground glass-like” increased parenchymal density, circumscribed
by a consolidation ring (Figure 5). It likely represents the disease progression towards
consolidation as described by Bernheim et al. [
19
], who detected it in 4% of the patients
studied at 6–12 days of infection.
Microorganisms 2021,9, 2037 5 of 19
Microorganisms 2021, 9, 2037 5 of 21
Figure 5. Reverse halo sign in right lower lobe in COVID-19.
Kuang et al. [20] conducted a study aimed to identify the CT differences between
H1N1 influenza pneumonia and COVID-19. Their results showed that the reverse halo
sign in COVID-19 pneumonia was present in 18.5% of cases, and that this sign was more
common than in H1N1 influenza pneumonia (p < 0.05).
2.6. Cavitation
Cavitation is quite rare in viral pneumonia and consequently also in SARS-CoV-2
and MERS-CoV pneumonias [21–23].
Zoumut et al. [24] investigated the development of lung cavitation in patients with
severe COVID-19 disease treated in ICU; a frequency of 11% was detected. They assumed
that cavitation was due to several factors such as bacterial and fungal coinfection,
immunosuppressive effects of glucocorticoids and tocilizumab, inflammatory state
induced by SARS-CoV-2, and thrombotic diathesis (Figure 6). This study also reported
that lung cavitation in patients with severe COVID-19 lung disease can occur and is
associated with secondary complications, such as hemoptysis and pneumothorax,
conferring a poor prognosis.
Figure 5. Reverse halo sign in right lower lobe in COVID-19.
Kuang et al. [
20
] conducted a study aimed to identify the CT differences between
H1N1 influenza pneumonia and COVID-19. Their results showed that the reverse halo
sign in COVID-19 pneumonia was present in 18.5% of cases, and that this sign was more
common than in H1N1 influenza pneumonia (p< 0.05).
2.6. Cavitation
Cavitation is quite rare in viral pneumonia and consequently also in SARS-CoV-2 and
MERS-CoV pneumonias [2123].
Zoumut et al. [
24
] investigated the development of lung cavitation in patients with
severe COVID-19 disease treated in ICU; a frequency of 11% was detected. They as-
sumed that cavitation was due to several factors such as bacterial and fungal coinfection,
immunosuppressive effects of glucocorticoids and tocilizumab, inflammatory state in-
duced by SARS-CoV-2, and thrombotic diathesis (Figure 6). This study also reported that
lung cavitation in patients with severe COVID-19 lung disease can occur and is associ-
ated with secondary complications, such as hemoptysis and pneumothorax, conferring a
poor prognosis.
2.7. Pneumothorax and Pneumomediastinum
As delineated by Vega et al. [
25
], a cough, typically present in COVID-19 disease,
is the cause of these two complications (Figures 7and 8). They illustrate three cases
of spontaneous pneumothorax and pneumomediastinum and argue that, although the
development of pneumothorax is usually secondary to barotrauma in patients in ICU, their
patients did not require, at diagnosis, assisted mechanical ventilation. They concluded that
in their cases the severity of the disease was associated with these rare complications.
Loffi et al. [
26
] identified 6 cases of spontaneous pneumomediastinum in
102 COVID-19
patients investigated with CT examination (6%). They asserted that spontaneous pneu-
momediastinum is a possible complication of severe COVID-19 pneumonia and can affect
patient management and clinical outcomes. In fact, in their experience “the concomitant
presentation of spontaneous pneumomediastinum and diffuse COVID-19 pneumonia
was associated with a severe clinical course characterized by sudden ARDS that required
aggressive management and early intubation in three patients”.
Table 1summarizes all the studies reported in Section 2: Adult “Atypical” and
“Complicated” Pulmonary COVID-19.
Microorganisms 2021,9, 2037 6 of 19
Microorganisms 2021, 9, 2037 6 of 21
Figure 6. Axial CT image of a 70-year-old female patient. Gross parenchymal consolidation with
central excavation suspected for superinfection is evident in the anterior segment of the right upper
lobe. In addition, reinforcing suspicion of superinfection, the study was negative for pulmonary
embolism.
2.7. Pneumothorax and Pneumomediastinum
As delineated by Vega et al. [25], a cough, typically present in COVID-19 disease, is
the cause of these two complications (Figures 7 and 8). They illustrate three cases of
spontaneous pneumothorax and pneumomediastinum and argue that, although the
development of pneumothorax is usually secondary to barotrauma in patients in ICU,
their patients did not require, at diagnosis, assisted mechanical ventilation. They
concluded that in their cases the severity of the disease was associated with these rare
complications.
Figure 7. Spontaneous right pneumothorax extended from apex to lung base. Axial (A); coronal (B); the right lung appears
hypo-expanded.
A B
Figure 6.
Axial CT image of a 70-year-old female patient. Gross parenchymal consolidation with cen-
tral excavation suspected for superinfection is evident in the anterior segment of the right upper lobe.
In addition, reinforcing suspicion of superinfection, the study was negative for
pulmonary embolism.
Figure 7.
Spontaneous right pneumothorax extended from apex to lung base. Axial (
A
); coronal (
B
); the right lung appears
hypo-expanded.
Microorganisms 2021, 9, 2037 7 of 21
Figure 8. Spontaneous pneumomediastinum in a COVID-19 patient.
Loffi et al. [26] identified 6 cases of spontaneous pneumomediastinum in 102 COVID-
19 patients investigated with CT examination (6%). They asserted that spontaneous
pneumomediastinum is a possible complication of severe COVID-19 pneumonia and can
affect patient management and clinical outcomes. In fact, in their experience “the
concomitant presentation of spontaneous pneumomediastinum and diffuse COVID-19
pneumonia was associated with a severe clinical course characterized by sudden ARDS
that required aggressive management and early intubation in three patients”.
Table 1 summarizes all the studies reported in Section 2: Adult “Atypical” and
“Complicated” Pulmonary COVID-19.
Table 1. Adults “atypical” and “complicated” pulmonary COVID-19.
Lymphadenopath
y
Pleural
Effusion
Pericardial
Effusion Bronchiectasis
Halo Sign/
Reverse Halo
Sign
Cavitation PNX*/
PNM*
Authors Total
Li et al. [8] 8.4% 4.8% 83
Grassi et al. [9] 54.8% 14.3% 16.7% 126
Xiao li et al.
[10] 43.5% 14.3% 154
Zhou et al. [11] 3.2% 62
Darwish et al.
[12] 13% 95
Ali Sabri et al.
[13] 7.9% 63
Romain A. et
al. [16] 41.3% 109
Devie A. et al.
[17] 25.3% 158
Wu and Chen
et al. [18] 13.8%/- 130
Bernheim et al.
[19] -/4% 121
Kuang et al.
[20] -/18.5% 405
Zoumut et al.
[24] 11% 110
Vega et al. [25]
(case rep.)
3 case of
PNX and
PNM
-
Figure 8. Spontaneous pneumomediastinum in a COVID-19 patient.
Microorganisms 2021,9, 2037 7 of 19
Table 1. Adults “atypical” and “complicated” pulmonary COVID-19.
Lymphadenopathy Pleural
Effusion
Pericardial
Effusion Bronchiectasis
Halo Sign/
Reverse
Halo Sign
Cavitation PNX*/
PNM*
Authors Total
Li et al. [8] 8.4% 4.8% 83
Grassi et al. [9] 54.8% 14.3% 16.7% 126
Xiao li et al. [10] 43.5% 14.3% 154
Zhou et al. [11] 3.2% 62
Darwish et al. [12] 13% 95
Ali Sabri et al. [13] 7.9% 63
Romain A. et al. [16] 41.3% 109
Devie A. et al. [17] 25.3% 158
Wu and Chen et al. [18] 13.8%/- 130
Bernheim et al. [19] -/4% 121
Kuang et al. [20] -/18.5% 405
Zoumut et al. [24] 11% 110
Vega et al. [25] (case rep.)
3 case of
PNX and
PNM
-
Loffi et al. [26] -/6% 102
*PNX: pneumothorax; *PNM: pneumomediastinum.
3. Children’s “Atypical” and “Complicated” Thoracic COVID-19 Manifestations
As in the adult case series, in pediatric patients COVID-19 pneumonia manifested
more frequently with some “typical” features, such as ground glass opacity (GGO), peri-
bronchial thickening, vascular engorgement and airspace consolidation [
27
30
]; as stated
also by the international consensus [
31
] regarding pediatric chest imaging. Atypical imag-
ing findings are represented by pleural effusion, atelectasis, nodules, linear opacities,
lymphadenopathy, pneumothorax and pneumomediastinum.
3.1. Pleural Effusion
Caro-Dominguez et al. [
27
] found pleural effusion in 7% of their cases,
Ugas-Charcape et al. [30]
described it in 6% and 13% of chest radiographs and CTs, respectively, while
Zhang et al. [29]
reported no cases of pleural effusion.
Pleural effusion (Figure 9) was found to be more significantly present in the frame of
MIS-C, a pathological multifactorial entity described below.
Microorganisms 2021, 9, 2037 8 of 21
Loffi et al. [26] -/6% 102
*PNX: pneumothorax; *PNM: pneumomediastinum.
3. Children’s “Atypical” and “Complicated” Thoracic COVID-19 Manifestations
As in the adult case series, in pediatric patients COVID-19 pneumonia manifested
more frequently with some “typical” features, such as ground glass opacity (GGO),
peribronchial thickening, vascular engorgement and airspace consolidation [27–30]; as
stated also by the international consensus [31] regarding pediatric chest imaging. Atypical
imaging findings are represented by pleural effusion, atelectasis, nodules, linear opacities,
lymphadenopathy, pneumothorax and pneumomediastinum.
3.1. Pleural Effusion
Caro-Dominguez et al. [27] found pleural effusion in 7% of their cases, Ugas-
Charcape et al. [30] described it in 6% and 13% of chest radiographs and CTs, respectively,
while Zhang et al. [29] reported no cases of pleural effusion.
Pleural effusion (Figure 9) was found to be more significantly present in the frame of
MIS-C, a pathological multifactorial entity described below.
Figure 9. Pleural effusion of the left lung with associated pulmonary atelectasis in a 10-year-old boy.
3.2. Atelectasis
The case series reports atelectasis in a few cases: 2% according to Caro-Dominguez et
al. [27] and Ugas-Charcape et al. [30]. This feature has been related to the presence of
associated pneumothorax and pleural effusion (Figure 9), or to an incorrect position of the
endotracheal tube [27].
3.3. Nodules and Linear Opacities
In a number of studies “nodules” refer to well-defined ground glass opacities.
Caro-Dominguez et al. [27] described pulmonary nodules in 25% of cases and linear
opacities in 33% of chest CT examinations. In a case series from Latin America [30] these
findings were reported in 9.7% and 15.6% of pediatric patients, respectively.
3.4. Lymphadenopathy
Lymphadenopathy, both hilar and mediastinal, as in the adult series, is an infrequent
feature in chest CT examinations. It was categorized as an atypical finding in the
international consensus statement of chest imaging in pediatric COVID-19 patients [31].
Figure 9.
Pleural effusion of the left lung with associated pulmonary atelectasis in a 10-year-old boy.
Microorganisms 2021,9, 2037 8 of 19
3.2. Atelectasis
The case series reports atelectasis in a few cases: 2% according to
Caro-Dominguez et al. [27]
and Ugas-Charcape et al. [
30
]. This feature has been related to the presence of associated
pneumothorax and pleural effusion (Figure 9), or to an incorrect position of the endotra-
cheal tube [27].
3.3. Nodules and Linear Opacities
In a number of studies “nodules” refer to well-defined ground glass opacities.
Caro-Dominguez et al. [
27
] described pulmonary nodules in 25% of cases and linear
opacities in 33% of chest CT examinations. In a case series from Latin America [
30
] these
findings were reported in 9.7% and 15.6% of pediatric patients, respectively.
3.4. Lymphadenopathy
Lymphadenopathy, both hilar and mediastinal, as in the adult series, is an infrequent
feature in chest CT examinations. It was categorized as an atypical finding in the inter-
national consensus statement of chest imaging in pediatric COVID-19 patients [
31
]. In a
subgroup of studies, it has low prevalence: 17% according to Caro-Dominguez et al. [
27
]
and 18% according to Zhang et al. [
29
]; other studies did not find any cases of thoracic
lymphadenopathy [22,30,32] in children affected by COVID-19.
3.5. Pneumothorax and Pneumomediastinum
Spontaneous pneumothorax and pneumomediastinum (Figure 10) are also very in-
frequent findings in pediatric COVID-19-related pneumonia: a study [
27
] reported pneu-
mothorax in 2% of cases, and a few case reports in the literature have described these
findings [33,34], usually in adolescents with severe disease.
Microorganisms 2021, 9, 2037 9 of 21
In a subgroup of studies, it has low prevalence: 17% according to Caro-Dominguez et al.
[27] and 18% according to Zhang et al. [29]; other studies did not find any cases of thoracic
lymphadenopathy [22,30,32] in children affected by COVID-19.
3.5. Pneumothorax and Pneumomediastinum
Spontaneous pneumothorax and pneumomediastinum (Figure 10) are also very
infrequent findings in pediatric COVID-19-related pneumonia: a study [27] reported
pneumothorax in 2% of cases, and a few case reports in the literature have described these
findings [33,34], usually in adolescents with severe disease.
(A) (B)
(C)
Figure 10. (AC): A 14-year-old girl with spontaneous pneumothorax and pneumomediastinum, in association with
extensive ground glass changes. In Figure 10C consolidation of the right lower lobe is noted.
Table 2 summarizes all the studies reported in Section 3: Children’s “Atypical” And
“Complicated” Thoracic COVID-19 Manifestations.
Table 2. Children’s “Atypical” and “Complicated” Thoracic COVID-19 Manifestations.
Lymphadenophaty
Pleural
Effusion Atelectasis Nodules/
Linear Opacities
PNX/
PNM
Authors Total
Dominguez et al. [27] 17% 7% 2% 25%/33% 2%/- 91
Zhang et al. [29] 18% 0% 41
Charcape et al. [30] 0% 13% 2% 9.7%/15.6% 140
Figure 10.
(
A
C
): A 14-year-old girl with spontaneous pneumothorax and pneumomediastinum, in association with
extensive ground glass changes. In Figure 10C consolidation of the right lower lobe is noted.
Microorganisms 2021,9, 2037 9 of 19
Table 2summarizes all the studies reported in Section 3: Children’s “Atypical” And
“Complicated” Thoracic COVID-19 Manifestations.
Table 2. Children’s “Atypical” and “Complicated” Thoracic COVID-19 Manifestations.
Lymphadenophaty Pleural
Effusion Atelectasis
Nodules/
Linear
Opacities
PNX/
PNM
Authors Total
Dominguez et al. [
27
]
17% 7% 2% 25%/33% 2%/- 91
Zhang et al. [29] 18% 0% 41
Charcape et al. [30] 0% 13% 2% 9.7%/15.6% 140
3.6. Cardiothoracic Mis-C
A hyperinflammatory immune-mediated shock syndrome has been recognized in chil-
dren aged <19 years were exposed to the severe acute respiratory syndrome coronavirus 2
(SARS-CoV-2). The WHO [
35
] and United States Center for Disease Control and Prevention
(CDC) [
36
] refer to this entity as Multisystem Inflammatory Syndrome in Children (MIS-C).
The diagnostic criteria of MIS-C have been defined by the WHO [
35
] and includes
biochemical evidence of elevated inflammatory markers, absence of other microbial causes
and evidence of organ dysfunction (e.g., hypotension, shock, myocardial dysfunction). At
the time of this report more than 4000 cases have been collected worldwide [36].
Affected patients present a wide spectrum of clinical findings consisting of fever,
headache, pain at the extremities, abdominal pain, vomiting and diarrhea, skin rash,
conjunctivitis and peripheral oedema, with variable severity, with a significant percentage
evolving to myocardial damage and cardiogenic, septic or toxic shock [
37
]. Laboratory
data measured in affected children show a marked pro-inflammatory state [38].
The post-viral hyperinflammatory process presumed to cause MIS-C results in unique
thoracic imaging abnormalities that differ from the classic manifestations of acute pediatric
COVID-19 infection [39].
Although radiological findings are not typical, they may be red flags for the diagnosis
of MIS-C when matched with clinical and laboratory data [40].
According to a number of studies the most common X-ray and CT findings are as follows:
perihilar opacity and peribronchial thickening; pleural effusion and
cardiomegaly [39,40]
;
atelectasis, airspace consolidation and diffuse ground glass appearance [4144].
Cardiac CT and MRI can also show heart failure with left ventricular systolic dysfunc-
tion, myocardial oedema, pericardial effusion and coronary artery dilatation [
40
43
], the
latter in the frame of the so-called Kawasaki-like disease [
45
], the well-known vasculitis
that affects the medium calibre vessels in children.
4. Adult “Abdominal” COVID-19
In recent times, the efforts of the international scientific community aimed to define
the abdominal manifestations of COVID-19, even if there is a small number of studies
published on this topic. Although the pathogenetic mechanisms have yet to be clarified,
we know that SARS-CoV-2 enters cells by exploiting the ACE-2 receptor which is widely
expressed in the GI tract, pancreas, biliary tract and vascular endothelium [
46
48
]. It
is also known that critical patients with COVID-19 have systemic coagulopathy and a
thrombotic diathesis supported by the important underlying inflammatory process [
48
51
].
Although pulmonary embolism is the most frequent thrombotic complication in these
patients, arterial thrombosis could be equally relevant and its presentation as acute aortic
occlusion would be evocative [
52
]. Baeza et al. [
53
] presented three cases of acute aortic
occlusion (AAO) and concluded that despite the pre-existence of risk factors in these
patients, there is likely an association between COVID-19 infection and the development of
a prothrombotic state leading to significant arterial complications (Figure 11).
Microorganisms 2021,9, 2037 10 of 19
Microorganisms 2021, 9, 2037 11 of 21
Figure 11. Case of acute aortic parietal thrombosis in patient affected by SARS-CoV-2 pneumonia. Image (A) shows the
lung’s involvement caused by COVID-19 pneumonia. Thromboembolic opacification defect of a segmental (anterior)
arterial branch for the right lower lobe is associated (B). (C) Axial images of subrenal acute aortic thrombosis. In coronal
image (D) is it possible to notice the acute aortic thrombosis which extends craniocaudally for about 6 cm. (E) Complete
resolution of aortic thrombosis after therapy.
This helps to clarify the pathogenetic mechanisms underlying pancreatitis, colitis and
abdominal infarction in COVID-19, although further studies are needed.
4.1. Kidney, Splenic and Intestinal Infarction
Goldberg-Stein et al. [46]
found splenic and renal infarction in 5% of COVID-19
patients investigated with CT examination, related to a state of hypercoagulation.
As described by Bhayana et al. [48] and Goldberg-Stein et al. [46] (reported also by
Tirumani et al. [54] and Lui et al. [55]) the pathogenetic mechanism underlying intestinal
infarcts in critical COVID-19 patients might be the thrombotic diathesis due to the
inflammatory response to the infection. On CT examination we can see mesenteric arterial
or venous filling defects, the “paper sheet wall” sign or the “target” sign with thickened
wall, constituted by hyperdense mucosa and hypodense submucosa. In the more
advanced stages this condition evolves with findings of hydro-aerial levels, and parietal
and portomesenteric pneumatosis (Figure 12). Tirumani et al. [54] observed the frequency
of intestinal infarction in 1/72 COVID-19 patients investigated with CT examination
(1.3%).
A B C
D E
Figure 11.
Case of acute aortic parietal thrombosis in patient affected by SARS-CoV-2 pneumonia. Image (
A
) shows the
lung’s involvement caused by COVID-19 pneumonia. Thromboembolic opacification defect of a segmental (anterior) arterial
branch for the right lower lobe is associated (
B
). (
C
) Axial images of subrenal acute aortic thrombosis. In coronal image
(D) is
it possible to notice the acute aortic thrombosis which extends craniocaudally for about 6 cm. (
E
) Complete resolution
of aortic thrombosis after therapy.
This helps to clarify the pathogenetic mechanisms underlying pancreatitis, colitis and
abdominal infarction in COVID-19, although further studies are needed.
4.1. Kidney, Splenic and Intestinal Infarction
Goldberg-Stein et al. [
46
] found splenic and renal infarction in 5% of COVID-19
patients investigated with CT examination, related to a state of hypercoagulation.
As described by Bhayana et al. [
48
] and Goldberg-Stein et al. [
46
] (reported also by
Tirumani et al. [
54
] and Lui et al. [
55
]) the pathogenetic mechanism underlying intestinal
infarcts in critical COVID-19 patients might be the thrombotic diathesis due to the inflam-
matory response to the infection. On CT examination we can see mesenteric arterial or
venous filling defects, the “paper sheet wall” sign or the “target” sign with thickened wall,
constituted by hyperdense mucosa and hypodense submucosa. In the more advanced
stages this condition evolves with findings of hydro-aerial levels, and parietal and portome-
senteric pneumatosis (Figure 12). Tirumani et al. [54] observed the frequency of intestinal
infarction in 1/72 COVID-19 patients investigated with CT examination (1.3%).
Microorganisms 2021,9, 2037 11 of 19
Microorganisms 2021, 9, 2037 12 of 21
Figure 12. Small area of splenic infarction (A); infarction of the cecum and right colon (BD): It is possible to notice the
marked dilatation of the ascending colon, with parietal pneumatosis and hydro-aerial levels. It was associated with
abdominal effusion in right subhepatic space and paracolic gutter which extended to the pelvic cavity.
4.2. Pancreatitis
Because of the expression of ACE-2 receptors also in pancreatic cells, pancreatitis can
occur in COVID-19 patients [46–48]
(Figure 13). Funt et al. [47] investigated the
presentation rate of pancreatitis in COVID-19 patients examined with CT, which
amounted to 1.5%. They searched for the most common causes of abdominal pain in two
groups of patients: COVID-19 positive and COVID-19 negative, respectively. In the subset
of acute disease, they documented: inflamed bowel, pancreatitis, pyelonephritis or cystitis
more frequently in COVID-19+ patients rather than in COVID-19- patients. As illustrated
by Wang et al. [56], pancreatitis presents in COVID-19 with a variable percentage ranging
from 12% of mild cases to 17% of severe cases. Bozdag A. et al. [57]
argue that in the
literature the pancreatitis diagnosis was based only on amylase and lipase elevation, while
the radiological findings were described only in case reports. In one case report
necrotizing pancreatitis was described [58].
A B C
D
Figure 12.
Small area of splenic infarction (
A
); infarction of the cecum and right colon (
B
D
): It is possible to notice
the marked dilatation of the ascending colon, with parietal pneumatosis and hydro-aerial levels. It was associated with
abdominal effusion in right subhepatic space and paracolic gutter which extended to the pelvic cavity.
4.2. Pancreatitis
Because of the expression of ACE-2 receptors also in pancreatic cells, pancreatitis
can occur in COVID-19 patients [
46
48
] (Figure 13). Funt et al. [
47
] investigated the
presentation rate of pancreatitis in COVID-19 patients examined with CT, which amounted
to 1.5%. They searched for the most common causes of abdominal pain in two groups of
patients: COVID-19 positive and COVID-19 negative, respectively. In the subset of acute
disease, they documented: inflamed bowel, pancreatitis, pyelonephritis or cystitis more
frequently in COVID-19+ patients rather than in COVID-19- patients. As illustrated by
Wang et al. [
56
], pancreatitis presents in COVID-19 with a variable percentage ranging
from 1–2% of mild cases to 17% of severe cases. Bozdag A. et al. [
57
] argue that in the
literature the pancreatitis diagnosis was based only on amylase and lipase elevation, while
the radiological findings were described only in case reports. In one case report necrotizing
pancreatitis was described [58].
4.3. Colitis, Enteritis
Goldberg-Stein et al. [
46
] reported that the abnormalities of the gastrointestinal tract
were the most common extra-pulmonary CT manifestations in COVID-19 patients. This
result was in agreement with those referred by Bhayana et al. [
48
], who found that 29%
of CT scans showed intestinal wall thickening involving the colon or small intestine. The
frequency of wall thickening in the gastrointestinal tract in the study by Goldberg Stein [
46
]
was lower (15%); they justify this difference by the fact that the intestinal wall thickening
may be relatively underestimated in the clinical setting compared to the experimental one
(Figure 14).
4.4. Cystitis and Cholecystitis
Goldberg-Stein et al. [
46
] and Funt et al. [
47
] reported cystitis in 5% and 4,1% of
COVID-19 cases, respectively, as an edematous thickening of the bladder wall with an
hyperdense aspect of the mucosa after contrast medium administration (Figure 15). In
Microorganisms 2021,9, 2037 12 of 19
the Goldberg-Stein et al. [
46
] paper, CT abnormal findings related to the gallbladder and
biliary system were reported in 25% of cases, including distention of the gallbladder, mural
oedema, and findings reported as possible or definite acute cholecystitis (Figure 15); 10% of
patients had bile duct dilatation. In two studies it is explained that there may be an unclear
SARS-CoV-2-induced cytopathic effect on hepatocytes, or an ACE-2 receptor-mediated
direct viral infection [
59
,
60
]. Since gallbladder wall oedema is a common finding in acute
hepatitis, and is an independent predictor of a more severe clinical course [
61
], it is possible
that gallbladder wall oedema seen in some of the patients is a reflex of hepatocellular
damage, either directly induced by SARS-CoV-2, or through an inflammatory response.
Further studies are needed to determine the link between COVID-19 positivity and biliary
and gallbladder pathologic implication.
Microorganisms 2021, 9, 2037 13 of 21
Figure 13. Pancreatitis. Enlarged and edematous pancreas especially at the head, with fat stranding
and peripancreatic fluid collection extending along the left anterior pararenal space.
4.3. Colitis, Enteritis
Goldberg-Stein et al. [46] reported that the abnormalities of the gastrointestinal tract
were the most common extra-pulmonary CT manifestations in COVID-19 patients. This
result was in agreement with those referred by Bhayana et al. [48], who found that 29% of
CT scans showed intestinal wall thickening involving the colon or small intestine. The
frequency of wall thickening in the gastrointestinal tract in the study by Goldberg Stein
[46] was lower (15%); they justify this difference by the fact that the intestinal wall
thickening may be relatively underestimated in the clinical setting compared to the
experimental one (Figure 14).
Figure 14. Colitis. Edematous thickening of the walls of the rectum-sigma with hyperdense aspects
of the mucosa showing contrast enhancement after administration of contrast medium. Intra-
abdominal effusion is associated.
Figure 13.
Pancreatitis. Enlarged and edematous pancreas especially at the head, with fat stranding
and peripancreatic fluid collection extending along the left anterior pararenal space.
Microorganisms 2021, 9, 2037 13 of 21
Figure 13. Pancreatitis. Enlarged and edematous pancreas especially at the head, with fat stranding
and peripancreatic fluid collection extending along the left anterior pararenal space.
4.3. Colitis, Enteritis
Goldberg-Stein et al. [46] reported that the abnormalities of the gastrointestinal tract
were the most common extra-pulmonary CT manifestations in COVID-19 patients. This
result was in agreement with those referred by Bhayana et al. [48], who found that 29% of
CT scans showed intestinal wall thickening involving the colon or small intestine. The
frequency of wall thickening in the gastrointestinal tract in the study by Goldberg Stein
[46] was lower (15%); they justify this difference by the fact that the intestinal wall
thickening may be relatively underestimated in the clinical setting compared to the
experimental one (Figure 14).
Figure 14. Colitis. Edematous thickening of the walls of the rectum-sigma with hyperdense aspects
of the mucosa showing contrast enhancement after administration of contrast medium. Intra-
abdominal effusion is associated.
Figure 14.
Colitis. Edematous thickening of the walls of the rectum-sigma with hyperdense aspects of
the mucosa showing contrast enhancement after administration of contrast medium. Intra-abdominal
effusion is associated.
Microorganisms 2021,9, 2037 13 of 19
Microorganisms 2021, 9, 2037 14 of 21
4.4. Cystitis and Cholecystitis
Goldberg-Stein et al. [46] and Funt et al. [47] reported cystitis in 5% and 4,1% of
COVID-19 cases, respectively, as an edematous thickening of the bladder wall with an
hyperdense aspect of the mucosa after contrast medium administration (Figure 15). In the
Goldberg-Stein et al. [46]
paper, CT abnormal findings related to the gallbladder and
biliary system were reported in 25% of cases, including distention of the gallbladder,
mural oedema, and findings reported as possible or definite acute cholecystitis (Figure
15); 10% of patients had bile duct dilatation. In two studies it is explained that there may
be an unclear SARS-CoV-2-induced cytopathic effect on hepatocytes, or an ACE-2
receptor-mediated direct viral infection [59,60]. Since gallbladder wall oedema is a
common finding in acute hepatitis, and is an independent predictor of a more severe
clinical course [61], it is possible that gallbladder wall oedema seen in some of the patients
is a reflex of hepatocellular damage, either directly induced by SARS-CoV-2, or through
an inflammatory response. Further studies are needed to determine the link between
COVID-19 positivity and biliary and gallbladder pathologic implication.
Figure 15. (A) Cholecystitis and (B) cystitis.
Table 3 summarizes all the studies reported in the Section 4: Adult “Abdominal”
COVID-19.
Table 3. Adults “Abdominal” COVID-19.
Acute Aortic
Occlusion
(AAO)
Kidney/Splen
ic/Intestinal
Infarction
Pancreatitis
Bowel
Thickening
(Colitis/Enteri
tis)
Cystitis
Cholecystitis
and Biliary
System
Manifestation
Authors Total
Goldberg
Stein et al.
[46]
5%/5%/- 15% 5% 25% 80
Stacey Funt
et al. [47] 1.5% 6.8% 4.1% 338
Bhayana et
al. [48] 2.4% 29% 42
Baeza et al.
[53] (case
rep)
3 cases -
A B
Figure 15. (A) Cholecystitis and (B) cystitis.
Table 3summarizes all the studies reported in the Section 4: Adult “Abdominal”
COVID-19.
Table 3. Adults “Abdominal” COVID-19.
Acute
Aortic
Occlusion
(AAO)
Kidney/Splenic/Intestinal
Infarction Pancreatitis Bowel Thickening
(Colitis/Enteritis) Cystitis
Cholecystitis
and Biliary
System
Manifestation
Authors Total
Goldberg Stein et al. [46] 5%/5%/- 15% 5% 25% 80
Stacey Funt et al. [47] 1.5% 6.8% 4.1% 338
Bhayana et al. [48] 2.4% 29% 42
Baeza et al. [53] (case rep) 3 cases -
Sree Tirumani et al [54] 1.3%/-/1.3% 1.3% 72
5. Pediatric “Abdominal” COVID-19 Manifestations
Abdominal manifestations of COVID-19 in children include mainly gastrointestinal
(GI), hepatobiliary and pancreatic involvement. Multisystem inflammatory syndrome in
children (MIS-C) is a complex entity that usually involves the gastrointestinal tract.
5.1. Gastrointestinal Manifestations
As explained above, SARS-CoV-2 enters cells via the angiotensin-converting enzyme-2
(ACE-2) receptor, which is abundantly expressed on lung cells, but also on many extra-
pulmonary tissues, including gastrointestinal (GI) tract, heart, liver, and kidney [62].
A number of studies have tried to estimate the prevalence of gastroenteric involvement
in COVID-19 infection in children, which is matter of debate: Miller et al. [
63
] showed
that gastrointestinal manifestations were present in 84.1% of children admitted to the
hospital and were more often associated with fever and rash; Akobeng et al. [
64
] in a meta-
analysis including 280 children from 9 studies estimated that the pooled prevalence of
gastrointestinal manifestations was 22.8%, with diarrhea as the most common presentation
(12.4%), followed by vomiting (10.3%) and abdominal pain (5.4%).
GI signs and symptoms appear characteristically as presenting features of SARS-CoV-
2-related multisystem inflammatory syndrome in children (MIS-C), a condition described
below [63].
Little is known about typical imaging findings in COVID-19 pediatric patients with
GI symptoms. Abdominal ultrasonography, computed tomography or magnetic resonance
imaging may be taken into consideration in patients with a severe course of disease or
relevant blood test alterations. Miller et al. [
63
] collected images from 15 patients with
Microorganisms 2021,9, 2037 14 of 19
GI symptoms, finding: mesenteric adenitis, biliary sludge or acalculous cholecystitis, and
ascites. In three patients, ultrasonography or magnetic resonance imaging showed bowel
wall thickening.
Tullie et al. [
65
] found on abdominal ultrasound the presence of lymphadenopathy,
inflammatory fat throughout the mesentery, and thickening of the terminal ileum, that
were confirmed with CT examination when performed.
Less frequent manifestations of GI SARS-CoV-2 involvement are reported in the
literature, consisting mainly of acute appendicitis, phlegmonous ileocolitis, intussusception,
pneumatosis intestinalis and protein losing enteropathy [66].
5.2. Hepatobiliary and Pancreatic Involvement
A study demonstrated that the distribution of ACE-2 is peculiar; it is highly expressed
in the endothelial layer of small blood vessels but not in the sinusoidal endothelium [
67
].
Its concentration on the surface of cholangiocytes is higher than of the hepatocyte surface
and is similar to the type II lungs alveolar cells [
68
]. SARS-CoV-2 may have the ability to
infect cholangiocytes via the ACE-2 receptor and directly dysregulate liver function [
67
].
Moreover, the induced intestinal inflammation impairs the intestinal mucosal barrier,
allowing easy access to the circulation and the possibility to reach and affect other organs,
including the liver [69].
Hepatitis was defined as an elevation of alanine aminotransferase (ALT) >40 and
aspartate aminotransferase (AST) >50, as these values fall above the 97
percentile for all
ages and both sexes, as defined by Bussler et al. [70].
A mild increase in liver enzymes is well described in COVID-19 pediatric patients,
with various results among studies, ranging from 13% to 50%; however, serious liver
dysfunction is uncommon [
71
]. Elevated aspartate aminotransferase levels (>50 UI/L) are
observed more frequently than alanine aminotransferase levels (>45 UI/L) [72].
Cantor et al. [
73
] described abdominal imaging performed on patients with hepatitis.
Abdominal ultrasounds showed abnormal liver-associated manifestation such as: sig-
nificant ascites, hepatomegaly or a thick-walled gallbladder. One of the two magnetic
resonance imaging studies showed ascites.
SARS-CoV-2 can affect both the exocrine and endocrine pancreas; an abnormal ele-
vation of amylase and lipase, together with glucose dysregulation and acute diabetes, are
described in pediatric patients with severe COVID-19 pneumonia, with development of
acute pancreatitis [74].
A few cases of pancreatic involvement have been reported in the literature in pe-
diatric patients. Samies et al. [
75
] illustrated three cases of pancreatitis in children af-
fected by COVID-19 that were diagnosed by laboratory tests and imaging (ultrasound or
CT examinations).
Both hepatitis and pancreatitis are observed more frequently in association with
MIS-C, as displayed below.
Table 4summarizes all the studies reported in Section 5: Pediatric “Abdominal”
COVID-19 Manifestations.
Table 4. Pediatric “Abdominal” COVID-19 Manifestation.
GI Involvement Hepato-Biliary
Involvement
Pancreatic
Involvement
Authors Total
Miller et al. [63] 20% 15
Tullie et al. [65]
(case rep) 5 cases -
Cantor et al. [73] 11% 44
Samie et al. [75]
(case rep) 3 cases -
Microorganisms 2021,9, 2037 15 of 19
5.3. MIS-C
The multisystem inflammatory syndrome in children (MIS-C), already mentioned
above [
35
38
], reported in patients under 19 years old who have a history of exposure to
SARS-CoV-2, has features that extensively involve the abdomen.
In regard to abdominal MIS-C, Caro-Dominguez et al. [
38
] found that the most com-
mon abnormalities in US, CT and MRI were free fluid (71%) and terminal ileum wall
thickening (57%) (Figure 16); other less common findings were hepatomegaly, right iliac
fossa lymphadenopathy, gallbladder wall oedema, gallbladder sludge, periportal oedema,
splenomegaly and haemorrhagic cystitis. According to Palabiyik et al. [
40
] the most con-
ventional US and CT findings were hepatomegaly and hepatosplenomegaly, followed by
periportal and pericholecystic wall oedema, mesenteric lymph nodes in the right lower
quadrant, free fluid in the abdomen, temporary invagination, echogenic kidneys and a
case of pancreatic alterations. Additionally, in the series of Hameed et al. [
43
], the most
common US and CT abdominal findings were represented by anechoic free fluid (53%), lo-
calized inflammatory change within the right iliac fossa (47%), a combination of echogenic
expanded mesenteric fat (37%), and multiple mildly enlarged lymph nodes in 47% of cases.
Microorganisms 2021, 9, 2037 17 of 21
(A) (B)
(C)
Figure 16. An 11-year-old patient with MIS-C. (AC): Abdominal effusion with cecum and sigma hyper enhancing wall
thickening.
6. Conclusions
In conclusion, this pictorial review shows the multiple aspects of COVID-19 infection
which make it a multi-organ disease. These aspects must be known and investigated to
obtain the best stratification and ensure optimal treatment for the patient. In fact, although
lymphadenopathies, pleural and pericardial effusion, bronchiectases, halo sign, reverse
halo sign and cavitations are notoriously associated with bacterial and fungal pneumonia,
our review aims to underline (through the scientific data reported), that these
manifestations are found in a non-negligible percentage of COVID-19 cases. Furthermore,
these atypical thoracic and gastrointestinal manifestations are associated with more
severe clinical settings, with systemic involvement and poor prognosis. We believe that
these findings can give a real clinical contribution by helping the clinicians to recognize
COVID-19 “red flags” associated with worse scenarios. CT is the best imaging method in
this environment, because it can be used to assess the progression of the disease and the
multisystem involvement.
Author Contributions: Conceptualization, A.S. (Arnaldo Scardapane) and C.M.; methodology, A.S.
(Arnaldo Scardapane); software M.D.C.; validation A.G., A.A.S.I. and A.S. (Antonello Sacco); formal
Figure 16.
An 11-year-old patient with MIS-C. (
A
C
): Abdominal effusion with cecum and sigma hyper enhancing
wall thickening.
Microorganisms 2021,9, 2037 16 of 19
6. Conclusions
In conclusion, this pictorial review shows the multiple aspects of COVID-19 infection
which make it a multi-organ disease. These aspects must be known and investigated
to obtain the best stratification and ensure optimal treatment for the patient. In fact,
although lymphadenopathies, pleural and pericardial effusion, bronchiectases, halo sign,
reverse halo sign and cavitations are notoriously associated with bacterial and fungal
pneumonia, our review aims to underline (through the scientific data reported), that these
manifestations are found in a non-negligible percentage of COVID-19 cases. Furthermore,
these atypical thoracic and gastrointestinal manifestations are associated with more severe
clinical settings, with systemic involvement and poor prognosis. We believe that these
findings can give a real clinical contribution by helping the clinicians to recognize COVID-
19 “red flags” associated with worse scenarios. CT is the best imaging method in this
environment, because it can be used to assess the progression of the disease and the
multisystem involvement.
Author Contributions:
Conceptualization, A.S. (Arnaldo Scardapane) and C.M.; methodology, A.S.
(Arnaldo Scardapane); software M.D.C.; validation A.G., A.A.S.I. and A.S. (Antonello Sacco); formal
analysis, P.P.; investigation M.F. and F.L.; resources A.A.S.I.; data curation M.F.; writing-original
draft preparation C.M. and A.S. (Arnaldo Scardapane); writing-review and editing C.M. and F.L.;
visualization, M.F., M.C. and G.S.; supervision, A.S. (Arnaldo Scardapane); All authors have read
and agreed to the published version of the manuscript..
Funding: This research received no external funding.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement:
Informed consent was obtained from all subjects involved in cases
reported in this review.
Data Availability Statement:
The authors confirm that the data supporting the findings of this
review are available within the article and its references list.
Conflicts of Interest: The authors declare no conflict of interest.
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... The findings were described according to the Fleischner Society glossary and in accordance with the article from Morelli, C., 'The Multifaceted COVID-19: CT Aspects of Its Atypical Pulmonary and Abdominal Manifestations and Complications in Adults and Children. A Pictorial Review' [21]. ...
... Following the current literature [21], we considered COVID-19 CT manifestations as typical and atypical (such as pleural effusion); moreover, we chose to evaluate the pulmonary involvement (expressed by the semiquantitative CT score) and the extent of disease to both lungs. Similarly to current reports [21], the bilateral lung involvement was depicted. ...
... Following the current literature [21], we considered COVID-19 CT manifestations as typical and atypical (such as pleural effusion); moreover, we chose to evaluate the pulmonary involvement (expressed by the semiquantitative CT score) and the extent of disease to both lungs. Similarly to current reports [21], the bilateral lung involvement was depicted. ...
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... In children, SARS-CoV-2 may lead to atypical skin manifestations, such as Kawasakilike disease [69][70][71]. From data reported in the scientific literature, in pediatric and adolescent ages, there seems to be a link between SARS-CoV-2 infection and a rare syndrome, MIS-C Kawasaki-like syndrome, that is similar to Kawasaki disease with other characteristics [72]. MIS-C differs from Kawasaki syndrome by being more severe at onset, by the presence of gastrointestinal symptoms (diarrhea, abdominal pain) or respiratory and pulmonary symptoms (cough, dyspnea) and the presence of inflammatory myopericarditis [73,74]. ...
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Background The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), which resulted in the worldwide coronavirus disease 2019 (COVID-19) pandemic of 2020, has particularly affected Latin America.Objective The purpose of the study was to analyze the imaging findings of pulmonary COVID-19 in a large pediatric series.Materials and methodsChildren with SARS-CoV-2 infection confirmed by either quantitative reverse transcription-polymerase chain reaction from nasopharyngeal swabs or presence of circulating immunoglobulin M (IgM) antibodies and who underwent chest radiograph or CT or both were included in this retrospective multicenter study. Three pediatric radiologists independently reviewed radiographs and CTs to identify the presence, localization, distribution and extension of pulmonary lesions.ResultsWe included 140 children (71 female; median age 6.3 years, interquartile range 1.6–12.1 years) in the study. Peribronchial thickening (93%), ground-glass opacities (79%) and vascular engorgement (63%) were the most frequent findings on 131 radiographs. Ground-glass opacities (91%), vascular engorgement (84%) and peribronchial thickening (72%) were the most frequent findings on 32 CTs. Peribronchial thickening (100%), ground-glass opacities (83%) and pulmonary vascular engorgement (79%) were common radiograph findings in asymptomatic children (n=25). Ground-glass opacity and consolidation were significantly higher in children who needed intensive care admission or died (92% and 48%), in contrast with children with a favorable outcome (71% and 24%, respectively; P<0.05).Conclusion Asymptomatic children and those with mild symptoms of COVID-19 showed mainly peribronchial thickening, ground-glass opacities and pulmonary vascular engorgement on radiographs. Ground-glass opacity and consolidation were more common in children who required intensive care admission or died.
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The World Health Organization defines the multisystem inflammatory syndrome in children (MIS-C) as a new syndrome reported in patients aged < 19 years old who have a history of exposure to SARS-CoV-2. The onset of this syndrome is characterized by persistent fever that is associated with lethargy, abdominal pain, vomiting and/or diarrhea, and, less frequently, rash and conjunctivitis. The course and severity of the signs and symptoms vary; in some children, MIS-C worsens rapidly and can lead to hypotension, cariogenic shock, or even damage to multiple organs. The characteristic laboratory findings are elevated markers of inflammation and heart dysfunction. The most common radiological findings are cardiomegaly, pleural effusion, signs of heart failure, ascites, and inflammatory changes in the right iliac fossa. In the context of the current COVID-19 pandemic, radiologists need to know the clinical, laboratory, and radiological characteristics of this syndrome to ensure the correct diagnosis.
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Purpose: The aim of this study was to evaluate how chest computed tomography (CT) can predict pejorative evolution in COVID-19 patients. Material and methods: Data on 349 consecutive patients who underwent a chest CT either for severe suspected COVID-19 pneumonia or clinical aggravation and with COVID-19 were retrospectively analysed. In total, 109 had laboratory-confirmed COVID-19 infection by a positive reverse-transcription polymerase chain reaction (RT-PCR) and were included. The main outcomes for pejorative evolution were death and the need for invasive endotracheal ventilation (IEV). All the CT images were retrospectively reviewed, to analyse the CT signs and semiologic patterns of pulmonary involvement. Results: Among the 109 COVID-19 patients, 73 (67%) had severe symptoms of COVID-19, 28 (25.7%) needed an IEV, and 11 (10.1%) died. The following signs were significantly associated with both mortality and need for IEV: traction bronchiectasis and total affected lung volume ≥ 50% (p < 10-3). Other CT signs were only associated with the need of IEV: vascular dilatation, air bubble sign, peribronchovascular thickening, interlobular thickening, and number of involved lobes ≥ 4 (p < 10-3). Conclusions: On a chest CT performed during the first week of the symptoms, the presence of traction bronchiectasis and high values of affected lung volume are associated with the need for IEV, and with mortality, in COVID-19 patients.
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Resumen El síndrome inflamatorio multisistémico pediátrico vinculado a la COVID-19 (SIM-PedS) es, según la Organización Mundial de la Salud, un nuevo síndrome descrito en pacientes menores de 19 años con historia previa de exposición a SARS-CoV-2. La presentación inicial de este síndrome se caracteriza por fiebre persistente que asocia debilidad, dolor abdominal, vómitos y/o diarrea. Menos frecuentemente los pacientes pueden presentar también erupción cutánea y conjuntivitis. El cuadro clínico tiene expresividad y evolución variables, por lo que algunos pacientes pediátricos afectados pueden empeorar rápidamente, desarrollando desde hipotensión y shock cardiogénico a daño multiorgánico. Los hallazgos analíticos característicos del síndrome consisten en elevación de marcadores inflamatorios y disfunción cardíaca. Los hallazgos radiológicos más frecuentes son cardiomegalia, derrame pleural, signos de insuficiencia cardíaca, ascitis y cambios inflamatorios en la fosa ilíaca derecha. En la pandemia actual por COVID-19 es necesario que el radiólogo conozca las características clínico-analíticas y radiológicas de este síndrome para realizar un correcto diagnóstico.