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Jinxin Liu

Xiaoping Tang
Chunliang Lei
Editors

Atlas of Chest Imaging


in COVID-19 Patients
Atlas of Chest Imaging in COVID-19 Patients
Jinxin Liu • Xiaoping Tang • Chunliang Lei
Editors

Atlas of Chest Imaging


in COVID-19 Patients
Editors
Jinxin Liu Xiaoping Tang
Department of Radiology Department of Infectious Diseases
Guangzhou Eighth People's Hospital, Guangzhou Eighth People's Hospital,
Guangzhou Medical University Guangzhou Medical University
Guangzhou, China Guangzhou, China

Chunliang Lei
Department of Infectious Diseases
Guangzhou Eighth People's Hospital,
Guangzhou Medical University
Guangzhou, China

ISBN 978-981-16-1081-3    ISBN 978-981-16-1082-0 (eBook)


https://doi.org/10.1007/978-981-16-1082-0

Jointly published with Tsinghua University Press

© The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021
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Foreword

The first glimpse of this book Atlas of Chest Imaging in COVID-19 Patient, which is edited by
Jinxin Liu, Xiaoping Tang, and Chunliang Lei from the Guangzhou Eighth People’s Hospital,
sent my thoughts back to early 2003, when a comprehensive book named Chest Imaging
Diagnostic Altas of SARS was published in which I wrote the preface and contributed as the
chief reviewer. Now, 17 years after the 2003 SARS outbreak, I am very delighted to know that
the same three anti-SARS heroes in 2003 accomplished such a comprehensive book with high-­
resolution images about COVID-19 in such a short time. This book embodies the hard work of
all medical personnel, especially imaging medical workers, in the Guangzhou Eighth People’s
Hospital. This book summarized their hard-won, precious, and encyclopedic imaging data
about COVID-19 patients in different conditions. It was also a testimony of their dedication to
the development of science. I express my sincere gratitude to them for their scientific attitude
in seeking truth from facts.
The book has the following features:
Firstly, chest CT and X-ray data which are extensively collected from COVID-19 patients
at different stages (including early stage, progressive stage, peak stage, and absorption stage)
provide an imaging reference covering the entire disease course to the readers and will help
readers to establish a better understanding of how the disease evolves and will guide the clini-
cal diagnosis and treatment as well.
Secondly, the chest CT images of some cases finally confirmed by multiple nucleic acid
tests and of different cases occurred in one family were presented, which strongly confirmed
the important role of chest CT in the diagnosis of COVID-19 pneumonia.
Thirdly, the follow-up CT examinations of COVID-19 patients who were CT normal during
the first examination recorded their lung imaging changes over the whole disease course and
emphasized the necessity and importance of multiple CT reexaminations for early patient
identification and diagnosis, isolation, and treatment for suspected and confirmed patients. In
addition, chest CT images of confirmed COVID-19 patients during the follow-up stage revealed
that over 90% lung lesions could be completely absorbed (or only a slight focal linear opacity
remained), which demonstrates that COVID-19 pneumonia is not only preventable and con-
trollable but curable.
I believe that this book can provide an important reference for medical workers and research-
ers in the clinical diagnosis, assessment of disease changes, and prognosis about COVID-19
pneumonia.
I would like to express my gratitude to the medical workers who have worked hard and
contributed to this book.

Nanshan Zhong
State Key Laboratory of Respiratory Disease
National Clinical Research Center for Respiratory Disease
Guangzhou Institute of Respiratory Health
First Affiliated Hospital of Guangzhou Medical University
Guangzhou, China

v
Preface

Life is like a dream. A scene like the SARS outbreak in 2003 which reoccurs countless times
in my dream now occurred 17 years later in reality at almost the same season in early 2020. For
us who once witnessed the SARS outbreak, and experienced and survived the hard and war-­
like times in 2003, our first reaction after we realized that an infectious “unknown pneumonia”
extremely similar to SARS, named as COVID-19 now, emerged was that of anxiety and con-
cern. We clearly know that the disease would cause severe social consequences once out of
control. What we could do was to reallocate and train personnel, to prepare enough medicines
and medical supplies, and to empty the occupied beds and backup isolation wards. We aimed
to maximally protect the whole Guangzhou population from suffering the COVID-19 disease
by admitting and treating the patients and by curing their diseases. With no delay, the
Guangzhou Eighth People’s Hospital arranged an emergency meeting which was called “pre-
paratory meeting for admission and treatment of pneumonia of unknown cause” on January 6,
2020. Right after the meeting, the whole hospital immediately entered a state of preparation.
On January 20, 2020, the hospital issued an emergency notice that required all staff to cancel
their coming festival holidays and to stand by on call in Guangzhou. On the same day, the
wards started to accept confirmed and suspected COVID-19 patients. The first batch of CT
examinations were conducted on January 22. Seven of all eight patients who received CT
examinations had typical imaging manifestations. By March 2, a total of 402 confirmed and
suspected patients had been admitted, 295 (including 46 cases of severe illness, 15 cases of
critical illness, and 1 case of death) were confirmed, and 232 cases were cured and discharged
from hospital; no medical personnel were infected.
No one can escape by sheer luck when in front of a pandemic. I had the same feeling and
agreed that “COVID-19 is still raging, we don’t know how many people will die or how many
families will never see the light of tomorrow from now on” in a news report when I knew that
professor Shunfang Wang, the wife of my supervisor, who once worked in Renmin Hospital of
Wuhan University, died of COVID-19 on February 26. She died only 5 days from confirmed
diagnosis. May there be no novel coronavirus and no pain in heaven.
Just as professor Nanshan Zhong, one academician of the Chinese Engineering Academy,
said, our understanding of COVID-19 is “just a preliminary understanding” and there are still
many unknowns to be explored and studied. Here, I would like to mention the other two elder
seniors who deserve our respect. One is professor Jincheng Chen from Jinan University; the
other is professor Xuelin Zhang from Southern Medical University. In order to understand the
imaging characteristics of SARS patients, they, regardless of their own safety, made a special
trip to the Eighth People’s Hospital of Guangzhou to check right after the SARS outbreak in
2003. They read the chest radiographs of all confirmed patients and gave us a lot of sugges-
tions. Their rigorousness in science and truth-seeking spirit are worthy of our learning and
inheritance.
This book is compiled on the basis of our consistent principles: data authenticity and com-
pleteness. We also provide our comments, insights, and interpretations after we have studied
the images and the disease evolution.
We collected the image data of 295 confirmed COVID-19 cases in our Guangzhou Eighth
People’s Hospital and included 922 images from 82 selected and typical cases in this atlas.

vii
viii Preface

This book covered the imaging manifestations of the confirmed COVID-19 cases in the onset
of the early stage, early stage, progression, and absorption stage. In particular, special chest
imaging data from first viral RNA test negative patients, from first CT test negative patients,
and from family gathering history confirmed patients are included in the atlas. They can serve
as references for our medical peers and aid their diagnosis and research.
We really wish to express our gratitude to Prof. Nanshan Zhong, academician of the Chinese
Engineering Academy, who wrote the preface for the atlas for his chief reviewing and detailed
suggestions.

Guangzhou, China Jinxin Liu


Contents

1 Overview ���������������������������������������������������������������������������������������������������������������������   1


Jing Qu, Lin Lin, Shuyi Xie, Feng Li, Jinxin Liu, Wanhua Guan,
Zhiping Zhang, Qingxin Gan, Chengcheng Yu, Rui Jiang, Zhoukun Ling,
Yanhong Yang, and Xiaoping Tang
2 Common CT Features of COVID-19 Pneumonia ���������������������������������������������������   9
Chengcheng Yu, Wanhua Guan, Shuijiang Cai, and Fei Shan
3 CT Features of Early COVID-19 Pneumonia (PCR-Positive) �������������������������������  17
Zhiping Zhang, Yan Ding, and Bihua Chen
4 CT Features of Intermediate Stage of COVID-19 Pneumonia�������������������������������  45
Lin Lin, Xi Xu, and Weiping Cai
5 CT Features of Late Stage of COVID-19 Pneumonia���������������������������������������������  71
Yanhong Yang, Peixu Wang, and Fengjuan Chen
6 Chest Features of Severe and Critical Patients with COVID-19 Pneumonia�������  91
Jing Qu, Xilong Deng, and Yanqing Ding
7 Role of CT and CT Features of Suspected COVID-19 Patients
(PCR Negative)����������������������������������������������������������������������������������������������������������� 115
Qingxin Gan, Tianli Hu, and Songfeng Jiang
8 Follow-Up CT of Patients with First Negative CT
But Positive PCR for COVID-19������������������������������������������������������������������������������� 137
Zhoukun Ling, Deyang Huang, and Chunliang Lei
9 Imaging Analysis of Family Clustering COVID-19������������������������������������������������� 163
Rui Jiang, Xiaoneng Mo, and Yueping Li
10 Residual CT Features in Recovery Stage of COVID-19 Pneumonia��������������������� 179
Yanhong Yang, Lieguang Zhang, Haiyan Shi, and Sufang Tian
11 CT Features and Pathological Analysis of COVID-19 Death��������������������������������� 187
Jing Qu, Li Liang, Meiyan Liao, and Ying Liu

ix
List of Contributors

Shuijiang  Cai Guangzhou Eighth People’s Hospital, Guangzhou Medical University,


Guangzhou, China
Weiping  Cai Guangzhou Eighth People’s Hospital, Guangzhou Medical University,
Guangzhou, China
Bihua  Chen Guangzhou Eighth People’s Hospital, Guangzhou Medical University,
Guangzhou, China
Fengjuan  Chen Guangzhou Eighth People’s Hospital, Guangzhou Medical University,
Guangzhou, China
Xilong  Deng Guangzhou Eighth People’s Hospital, Guangzhou Medical University,
Guangzhou, China
Yan Ding  Guangzhou Eighth People’s Hospital, Guangzhou Medical University, Guangzhou,
China
Yanqing Ding  Nanfang Hospital, Southern Medical University, Guangzhou, China
Qingxin  Gan Guangzhou Eighth People’s Hospital, Guangzhou Medical University,
Guangzhou, China
Wanhua  Guan Guangzhou Eighth People’s Hospital, Guangzhou Medical University,
Guangzhou, China
Tianli Hu  Guangzhou Eighth People’s Hospital, Guangzhou Medical University, Guangzhou,
China
Deyang  Huang Guangzhou Eighth People’s Hospital, Guangzhou Medical University,
Guangzhou, China
Rui Jiang  Guangzhou Eighth People’s Hospital, Guangzhou Medical University, Guangzhou,
China
Songfeng  Jiang Guangzhou Eighth People’s Hospital, Guangzhou Medical University,
Guangzhou, China
Chunliang  Lei Guangzhou Eighth People’s Hospital, Guangzhou Medical University,
Guangzhou, China
Feng Li  Guangzhou Eighth People’s Hospital, Guangzhou Medical University, Guangzhou,
China
Yueping  Li Guangzhou Eighth People’s Hospital, Guangzhou Medical University,
Guangzhou, China
Li Liang  Nanfang Hospital, Southern Medical University, Guangzhou, China
Meiyan Liao  Zhongnan Hospital of Wuhan University, Wuhan, China

xi
xii List of Contributors

Lin Lin  Guangzhou Eighth People’s Hospital, Guangzhou Medical University, Wuhan, China
Zhoukun  Ling Guangzhou Eighth People’s Hospital, Guangzhou Medical University,
Guangzhou, China
Jinxin Liu  Guangzhou Eighth People’s Hospital, Guangzhou Medical University, Guangzhou,
China
Ying Liu  Guangzhou Eighth People’s Hospital, Guangzhou Medical University, Guangzhou,
China
Xiaoneng  Mo Guangzhou Eighth People’s Hospital, Guangzhou Medical University,
Guangzhou, China
Jing Qu  Guangzhou Eighth People’s Hospital, Guangzhou Medical University, Guangzhou,
China
Fei Shan  Shanghai Public Health Clinical Center, Fudan University, Shanghai, China
Haiyan  Shi Guangzhou Eighth People’s Hospital, Guangzhou Medical University,
Guangzhou, China
Xiaoping  Tang Guangzhou Eighth People’s Hospital, Guangzhou Medical University,
Guangzhou, China
Sufang Tian  Zhongnan Hospital of Wuhan University, Wuhan, China
Peixu  Wang Guangzhou Eighth People’s Hospital, Guangzhou Medical University,
Guangzhou, China
Shuyi Xie  Guangzhou Eighth People’s Hospital, Guangzhou Medical University, Guangzhou,
China
Xi Xu  The First Affiliated Hospital, Jinan University, Guangzhou, China
Yanhong  Yang Guangzhou Eighth People’s Hospital, Guangzhou Medical University,
Guangzhou, China
Chengcheng  Yu Guangzhou Eighth People’s Hospital, Guangzhou Medical University,
Guangzhou, China
Lieguang  Zhang Guangzhou Eighth People’s Hospital, Guangzhou Medical University,
Guangzhou, China
Zhiping  Zhang Guangzhou Eighth People’s Hospital, Guangzhou Medical University,
Guangzhou, China
Overview
1
Jing Qu, Lin Lin, Shuyi Xie, Feng Li, Jinxin Liu,
Wanhua Guan, Zhiping Zhang, Qingxin Gan,
Chengcheng Yu, Rui Jiang, Zhoukun Ling, Yanhong Yang,
and Xiaoping Tang

1.1 Introduction analysis revealed that COVID-19 patients were middle-aged


and older adults with no gender difference and that most
Coronavirus disease 19 (COVID-19), caused by severe acute COVID-­ 19 patients had a clear disease-related exposure
respiratory syndrome coronavirus 2 (SARS-CoV-2) infection, history. Similar to transmission of other respiratory viruses
has spread around the world with no sign of ceasing. Over 40 through respiratory droplets and close contact, SARS-CoV-2
million COVID-19 cases and more than 1 million fatal cases infection also exhibits a pattern of clustering distribution,
were reported by the end of October 2020, and the number is such as among familial members and relatives, in communi-
still increasing. The diagnosis of COVID-19 mainly relied on ties including neighborhoods, schools, and shared working
the laboratory viral RNA detection in upper respiratory sam- space; and in public areas including malls, restaurants, and
ples, such as throat and nasal swabs, because of their ease of transportation vehicles.
access. SARS-CoV-2 appears to be transmitted via respiratory
droplets and aerosols and contact with contaminated surface. 1. Source of Infection
Because the viral receptor ACE2 is expressed abundantly in the
lung epithelial cells, SARS-­CoV-­2 will easily establish infec- The SARS-CoV-2-infected patients are the main source
tion in the lung if inhaled in after a deep breath and then spread of infection, and they usually shed higher concentrations of
gradually from the bottom to the other part of the upper respira- virus within 5 days after onset. Notably, COVID-19 patients
tory tract. When throat and nasal samples are collected in this in the incubation period start to excrete virus before obvi-
time window, viral RNA detection will fail and present a nega- ous symptom onset and without seeking medical help, and
tive result. For a certain percentage of COVID-19 patients, the some patients are completely asymptomatic infectees, serv-
time window is so wide that the virus has caused lung damage ing unidentified viral reservoirs for rapid virus spreading.
long before it is detected in the throat samples. To overcome this
limitation, computed tomography (CT) of the chest is definitely 2. Means of Transmission
required as an alternative and complementary approach to diag-
nose and confirm virus infection through checking typical lung The main routes of SARS-CoV-2 transmission are
lesions when combined with a clear and close contact history reported to be through respiratory droplets, person-to-person
with a confirmed or highly suspected SARS-CoV-2 infectee. close contact, and contaminated items.
It is possible that the virus may spread through aerosols
under prolonged exposure to high concentrations of aerosols
1.2 Epidemiological Characteristics [1–4] in a relatively closed environment.
In addition, the live SARS-CoV-2 virus can be isolated
Over 500 COVID-19 patients (over 90% of all COVID-19 from feces or urine samples, and thus, viral contaminated
patients in Guangzhou City) were admitted in Guangzhou environment might also be a natural infection resource.
Eighth People’s Hospital on August 2020. Epidemiological
3. Susceptible Population
J. Qu · L. Lin · S. Xie · F. Li · J. Liu (*) · W. Guan · Z. Zhang ·
The whole population is generally susceptible since the
Q. Gan · C. Yu · R. Jiang · Z. Ling · Y. Yang · X. Tang
Guangzhou Eighth People’s Hospital, Guangzhou Medical virus originated from nature. Protective immunity may be
University, Guangzhou, China obtained through natural SARS-CoV-2 infection or through

© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 1
J. Liu et al. (eds.), Atlas of Chest Imaging in COVID-19 Patients, https://doi.org/10.1007/978-981-16-1082-0_1
2 J. Qu et al.

vaccination. However, how long this protection lasts is still hematopoietic cells were found to actively proliferate in some
under observation. individuals, while they were decreasing in other individuals,
and the ratio of granulocyte and erythrocyte was found to
increase. Hemophagocytosis was also occasionally observed.
1.3 Pathological Characteristics [1, 5–8]
3. Cardiovascular System
Although COVID-19 is mainly a pulmonary disease, it
can cause cardiac, dermatologic, hematological, hepatic, The disease could cause degeneration and necrosis in car-
neurological, renal, and other complications [9–17]. diomyocytes, along with interstitial congestion and edema.
Thromboembolic events were often observed in COVID-19 There was a slight infiltration of monocytes, lymphocytes,
patients and were reported to significantly increase the risk and/or neutrophils.
for critical COVID-19 patients. In the small vessels of major organs, endothelial cell
The imaging changes of COVID-19 pathogenesis in shedding and intimal or full-thickness inflammation could
major organs (excluding underlying disease lesions) were be seen. Mixed thrombosis, thromboembolism, and infarc-
discussed as follows. tion occurred in the corresponding part. Obvious thrombosis
was observed in the capillaries of the main organs.
1. Lungs

The lungs showed varying degrees of consolidation. The 1.4 General Clinical Manifestations [1, 18]
consolidation area mainly presented diffuse alveolar injury
and exudative alveolitis. Pulmonary disease in different The general clinical symptoms of COVID-19 include fever,
areas had become complex and varied, with old and new dry cough, fatigue, muscle soreness, headache, diarrhea etc.
lesions interlaced. Serous exudate, fibrinous exudate, and COVID-19 patients are classified as asymptomatic, mild,
hyaline membrane were found in the alveolar cavity. The moderate, severe, and critical patients based on clinical
exudate cells were mainly mononuclear, macrophages, and symptoms.
multinucleated giant cells. Type II alveolar epithelial cells The asymptomatic patients are only SARS-CoV-2 RNA
proliferate, and some cells were exfoliated. There were positive but has no sign of clinical symptoms. Only a small
occasional inclusions in type II alveolar epithelial cells and percentage of COVID-19 patients are asymptomatic.
macrophages. Hyperemia, edema, and infiltration of mono- Mild patients may present with low fever, slight fatigue,
cytes and lymphocytes could be seen in the alveolar septa. A smell and taste disorders, but no pneumonia. When patients
few alveoli were overfilled, alveolar compartments ruptured, have pneumonia, they are diagnosed as moderate COVID-­19.
and cysts formed. The bronchial epithelium of each level in Mild and moderate patients account for the majority of all
the lung partly fell off, while exudate and mucus could be COVID-19 patients.
seen in the cavity. Pulmonary vasculitis and thrombotic for- Some patients progressed to severe and even critical stage
mation (mixed thrombus, hyaline thrombus) appeared, and at approximately 1–2 weeks after symptom onset. They
thrombotic lung tissue tended to demonstrate focal pulmo- manifested as acute respiratory distress syndrome, septic
nary hemorrhage.In some patients with long-term disease, shock, hard-to-correct metabolic acidosis, blood coagulation
fibrinogen exuded in the alveoli formed cellulose, and the dysfunction, etc. [1]. Those critical COVID-19 patients are
organized cellulose caused diffuse thickening and fibrosis of elderly, people with chronic basic diseases, women in the
the alveolar walls. third trimester and perinatal period, and obese people.
SARS-CoV-2 particles could be seen in the cytoplasm of Symptoms in children were relatively mild. Some chil-
the bronchial mucosal epithelium and type II alveolar epithe- dren and newborns had atypical symptoms, such as vomit-
lial cells under electron microscopy. Immunohistochemical ing, diarrhea, and other gastrointestinal symptoms or only
staining revealed that some bronchial mucosal epithelium, lack of alertness and shortness of breath.
alveolar epithelial cells, and macrophages were SARS-­ COVID-19 children occasionally will have multisys-
CoV-­2 antigen immunostaining and nucleic acid test positive. tem inflammatory syndrome (MIS-C), similar to Kawasaki
disease, atypical Kawasaki disease, toxic shock syndrome,
2. Lymphatic and Hematopoietic Systems macrophage activation syndrome, etc., mostly during their
recovery period. The main symptoms are fever with rash,
Immunohistochemical staining revealed a decreased CD4+ nonsuppurative conjunctivitis, mucosal inflammation, hypo-
and CD8+ T cells in the spleen and lymph nodes. In lymph tension or shock, coagulation disorders, acute ­gastrointestinal
nodes, viral RNA were detected by in situ RNA staining, and symptoms, etc. Once it happens, the disease can deteriorate
macrophage was found by immunostaining. In bone marrow, rapidly in a short time.
1 Overview 3

1.5 Laboratory Examinations were detected, the results should be interpreted carefully for
the following reasons.
1.5.1 R
 outine Blood Cell Examination Not all SARS-CoV-2 antibodies are protective. SARS-­
and Biochemical Examinations CoV-­2 expresses multiple proteins, and all secreted proteins
can evoke antibodies. But antibodies against the receptor
binding domain (RBD) of S proteins which can prevent
In the early stages of infection, the peripheral white blood cell SARS-CoV-2 from binding to an entry receptor are gener-
counts and lymphocyte counts in most COVID-19 patients ally regarded as protective.
were in normal range or slightly decreased. C-reactive pro- How long the protective antibodies can last after dis-
tein (CRP) and erythrocyte sedimentation rate were elevated charge is still unknown. Until now, it is too early to claim
in most patients, and procalcitonin was usually normal. that one individual acquires long-term sterile immunity
Patients in the severe stage usually had substantially elevated when antibodies are detected. Indeed, reinfection cases have
D-dimer and progressively declining peripheral blood lym- been reported recently.
phocytes. Liver enzymes, lactate dehydrogenase, muscle
enzymes, and myoglobin in some patients increased; some
critically ill patients had increased troponin. 1.5.3 Etiological Examination

SARS-CoV-2 RNA is detected in the lung, upper respira-


1.5.2 Serological Examination tory and lower respiratory tracts, mouth, blood (occasional
in severe/critical patients), feces (seldom), and urine (rare).
1.5.2.1 Serological Diagnosis of SARS-CoV-2 However, because of easy access and availability, naso- and
Infection oropharyngeal swabs are widely used for SARS-CoV-2 viral
Serological Examination: Detecting SARS-CoV-2 specific RNA detection by real-time fluorescent reverse transcription
IgM and IgG antibodies was an easy and helpful test for clin- polymerase chain reaction (RT-PCR) and/or next-generation
ical diagnosis in the early phase of SARS-CoV-2 pandemic. sequencing (NGS). Viral detection in the lower respiratory tract
Because viral specific IgM and IgG generation requires sev- specimens (sputum or airway extracts) where high concentra-
eral days after viral infection, antibody testing could not pro- tions of virus exist is much easily and thus more accurate.
vide a reliable early diagnosis for those patients right after Viral RNA nucleic acid testing would be affected by
they are infected, typically within 1 week of onset. the course of disease and specimen collection procedure.
The specificity and sensitivity of IgM and IgG test itself Reliable detection reagent and standardized sample collec-
constrained their wide application. Endogenous interfering tion and process procedures will safeguard the detection
factors such as the presence of interfering substances (such as accuracy.
rheumatoid factor, heterophile antibodies, complement, and
lysozyme) from the host, specimen contamination (such as
hemolysis of specimens and environment pollutants) caused 1.6 Chest Imaging Examinations
by bacteria, and improper handling procedures (such as lon-
ger sample storage and incomplete coagulation) could affect Imaging examination is a critical alternative for early diagno-
the detection specificity. Importantly, SARS-CoV-2 infec- sis, for monitoring disease process, for assessing the severity
tion in a certain percentage of COVID-19 patients fails to of the disease, and for evaluating the patient recovery after
evoke viral specific IgM and IgG antibodies. Therefore, IgM viral RNA becomes negative [19].
and IgG tests have not been taken as a confirmed diagnosis
alone but are very beneficial for diagnosis when combined
with other factors, especially a clear epidemiological history. 1.6.1 Chest Radiographs
SARS-CoV-2 infection could be diagnosed by antibody
tests for (1) highly suspected COVID-19 patients based on In the early stage, some patients showed negative chest
clinical symptoms but with negative viral RNA results and X-ray signs. In some patients, the chest radiographs showed
for (2) convalesced COVID-19 patients with negative viral scattered high-density shadows in the lateral field of the
RNA results. lung, and a few patients showed diffuse distribution of
­ground-­glass opacities. The progress of the disease course in
1.5.2.2 Serologic Testing Protection Prediction some patients was relatively rapid, and the consolidation was
The expert panel recommended that serological testing could mainly seen in bilateral lower lobes. In a few patients, the
not be used to determine whether a person obtains protective lungs were “white lung” or similar to “white lung.” Pleural
immunity against SARS-CoV-2 infection. When antibodies effusion was rare.
4 J. Qu et al.

1.6.2 Chest CT [20–22] The clinical manifestations included fever and respira-
tory symptoms, accompanied with imaging manifestations
Early Period: The main CT findings were ground-glass of pneumonia.
opacification with or without thickening of the interlobu-
lar septum and dilated blood vessel crossing the lesion. 3. Severe type
Considering that the pathological changes were mainly
acute inflammation, the virus mainly invaded the epithelial Adults meet any of the following criteria:
cells of bronchiole mucosa and type II alveolar epithelial
cells (because the lesion was mainly distributed under the (a) Onset of shortness of breath, RR ≥ 30 times/min
pleura of the bilateral lung field), causing epithelial shed- (b) In the resting state, SpO2 (oxygen saturation) ≤93%
ding and inflammatory injury of the alveolar septal ves- when inhaling air
sels and finally resulting in serous fibrinous exudation and (c) Partial pressure of blood oxygen (PaO2)/oxygen absorp-
lymphocyte infiltration in the alveolar cavity. And there had tion (FiO2) ≤300 mmHg
been some progress in developing artificial intelligence (AI) (d) Patients with progressive clinical symptoms and whose
computer-aided systems for CT-based COVID-19 diagnosis pulmonary imaging showed lung infiltrates >50% within
[23]. 24–48 h
Progression Period: The mainly manifestations were
ground-glass opacities with consolidation and the change of A child meets any of the following criteria:
interstitium of the lungs, including interlobular septal thick-
ening, intralobular septal thickening, and subpleural line; (a) Sustained high fever for more than 3 days
moreover, “crazy-paving sign” was visible. The pathological (b) Onset of shortness of breath (<2 months old, RR ≥ 60
changes included diffuse intra-alveolar hemorrhage, fibrin- times/min; 2–12 months old, RR  ≥  50 times/min; 1–5
ous exudation, and interstitial inflammatory cell infiltration. years old, RR ≥ 40 times/min; >5 years old, RR ≥ 30
With the aggravation of lesions, mucus blockage occurred in times/min), excluding the effects of fever and crying
the bronchioles and terminal bronchioles, resulting in alveolar (c) In resting state, oxygen saturation ≤93% when inhaling
collapse. air
Severe Period: The most common manifestations were dif- (d) Assisted ventilation (alar flap, three-concave sign)
fuse multiple patchy consolidation; some cases manifest as (e) Lethargy and convulsions
“white lung.” The pathological changes included diffuse alveolar (f) Refusal of food or difficulty in feeding and signs of
damage, intra-alveolar edema, and hyaline membrane formation. dehydration
Absorption Period: After treatment, the lesions were
cleared in most patients. In addition, few fibrous lesions 4. Critical type
remain in the lungs of some patients.
The Distribution of Lesions: The lesions of two lungs One of the following conditions:
were mainly multiple, especially in the bilateral lower lobes.
The lesions were mainly distributed in the periphery of the (a) Respiratory failure and requiring mechanical
lung, and the development trend of the lesion was generally ventilation
from the periphery of the lung to the center of the bronchi. In (b) Septic shock
the course of the disease, the lesions in the lungs manifested (c) Patients with multiple organ dysfunction or failure who
as “growing and disappearing,” showing the coexistence of should be monitored in the intensive care unit (ICU)
multiple manifestations.
Others: Pleural effusion and lymphadenopathy were rare.
1.8 Differential Diagnosis

1.7 Clinical Classification [1, 24] 1. Mild COVID-19 symptoms should be distinguished from
upper respiratory tract infection caused by other viruses.
1. Mild type 2. COVID-19 was mainly differentiated from influenza

virus, adenovirus, respiratory syncytial virus, and other
The clinical symptoms were mild, and no manifestations
known viral pneumonia and mycoplasma pneumoniae
of pneumonia were found on imaging.
infection. Especially for suspected cases, rapid antigen
2. Moderate type detection and multiple PCR nucleic acid detection should
1 Overview 5

be adopted to detect common respiratory pathogens as far 2. Intravenous injection of COVID-19 human immunoglob-
as possible. ulin: it could be applied to ordinary and severe patients
3. It was necessary to distinguish from noninfectious dis- with rapid disease progression in an emergency.
eases, such as vasculitis, dermatomyositis, and organized 3. Tozumab: It could be used in patients with extensive
pneumonia. bilateral lung diseases and severe patients, and the level
4. When a rash or mucosal damage occurred in a child patient, of IL-6 will increase in laboratory tests. Pay attention to
it was necessary to differentiate from Kawasaki disease. allergic reactions. Tuberculosis and other active infection
were prohibited to use tozumab.

1.9 Treatment and Outcome 1.9.1.4 Glucocorticoid Therapy


For patients with gradual deterioration of oxygenation
1.9.1 Treatment index, rapid imaging progress, and excessive activation of
the body’s inflammatory response, short-term glucocorticoid
According to the condition to determine the treatment site: therapy should be given (generally recommended 3–5 days,
no more than 10 days). The recommended dose of gluco-
1. Suspected and confirmed cases should be isolated and corticoid was prednisolone 0.5–1 mg/kg/day. Due to immu-
treated in designated hospitals with effective isolation and nosuppressive effects, we should pay attention to the use of
protective conditions. Suspected cases should be isolated high-dose glucocorticoids, which may delay the removal of
in a single room. the virus.
2. Critical cases should be admitted to ICU as soon as

possible. 1.9.1.5 Treatment of Severe, Critical Cases
1. Treatment principle: Actively symptomatic treatment to
1.9.1.1 General Treatment prevent complications and secondary infections. Support
1. Maintain internal environmental stability with supportive organ functions in time.
treatment, and closely monitor vital signs, blood oxygen 2. Respiratory support includes oxygen inhalation by a nasal
saturation of the pinched fingers, etc. catheter or mask; transnasal high-flow oxygen therapy or
2. Monitor blood cells, urine, C-reactive protein (CRP), bio- noninvasive ventilation; invasive mechanical ventilation;
chemical indicators (liver enzymes, cardiac enzymes, kidney airway management; extracorporeal membrane oxygen-
function, etc.), and coagulation function. Perform arterial ation (ECMO).
blood gas analysis, and repeat chest imaging if necessary. 3. Circulatory support.
3. Take effective oxygen therapy measures in time accord- 4. Anticoagulation therapy.
ing to the changes in blood oxygen saturation. 5. Acute kidney injury and renal replacement therapy.
4. Antimicrobial therapy: Avoid inappropriate use of antimi- 6. Blood purification treatment.
crobial drugs, especially combinations of broad-spectrum 7. Other treatment measures may be considered, such as
antibacterial drugs. antiendotoxin medicine like Xuebijing. Intestinal micro-
ecological regulator could be used to maintain intestinal
1.9.1.2 Antiviral Therapy microecological balance and prevent secondary bacterial
Although antiviral drugs had not been found to be effec- infection. IVIG may be considered as appropriate in
tive after a rigorous “randomized, double-blind, placebo-­ severe or critical children cases. Patients with severe or
controlled study,” there was relatively consensus that the critical pregnancy should be actively terminated;
drugs with potential antiviral effect should be used in the C-­section is the first choice.
early stage of the disease, and it was recommended to focus
on the patients with severe risk factors and the tendency of
severe disease, such as interferon-alpha nebulized inhala- 1.9.1.6 Traditional Chinese Medical Treatment
tion, lopinavir/ritonavir, ribavirin, chloroquine phosphate, Traditional Chinese Medical Treatment (TCM) may be effec-
and Abidol. tive in treating COVID-19. Jinhua Qinggan (JHQG) granules
and Lianhua Qingwen (LHQW) capsules are recommended
1.9.1.3 Immunotherapy during medical observation; Lung Cleansing and Detoxifying
1. Convalescent plasma from individuals who had recovered Decoction (LCDD) is recommended for the treatment of
from SARS-CoV-2 infection [25, 26]: it was suitable for both severe and non-severe patients; Xuanfeibaidu (XFBD)
severe and critical patients with rapid disease progression. granules are recommended for treating moderate cases;
6 J. Qu et al.

while Huashibaidu (HSBD) and Xuebijing (XBJ) have been References


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Over 500 COVID-19 patients were admitted to Guangzhou issn.1673-­4777.2020.10.002.
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1 Overview 7

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24. Wu Z, McGoogan JM.  Characteristics of and important lessons
from the coronavirus disease 2019 (COVID-19) outbreak in China:
Common CT Features of COVID-19
Pneumonia 2
Chengcheng Yu, Wanhua Guan, Shuijiang Cai,
and Fei Shan

2.1 Introduction vascular bundles [3]. “Air bronchial sign” can be seen in
some lesions. The appearance of consolidation indicated
Since the outbreak of coronavirus disease (COVID-19) the progression of COVID-19 pneumonia.
pneumonia in January 2020, collections of imaging features 3. Interstitial changes. Thickening of the lobular interstitia,
from COVID-19 patients have been documented. Diagnosis interlobular interstitia, and subpleural interstitium can be
of COVID-19 pneumonia is usually made by a combination seen in both lungs, which manifested as reticular or linear
of epidemiology of close contact history, clinical symptoms, opacities in the background of ground-glass opacities on
and imaging features. In this chapter, we described the typi- chest CT. The appearance of these features may be asso-
cal features of computed tomography (CT) imaging from ciated with interstitial lymphocyte infiltration [4]; “crazy-­
COVID-19 pneumonia, and we hope they can be helpful in paving sign” and “honeycomb-like” shadow can be seen
improving the diagnostic accuracy. in few patients.
4. Pleura thickening. The thickening of the pleura adjacent
1. Ground-glass opacity. Ground-glass density was the most to the lesion was commonly observed.
common feature of COVID-19 pneumonia which can be 5. Pleural effusion and lymphadenopathy occurred rarely.
presented as single, multiple nodular, or patchy shadows on
chest CT.  Besides, the unclear boundary and thickened
blood vessels can be seen [1]. Most lesions are mainly dis- 2.2 Ground-Glass Opacity
tributed in the subpleural area and/or the periphery of both
lung fields. The reasons for above features may be the thick- At the early stage of COVID-19 pneumonia, CT scans show
ening of the alveolar interval due to infiltration of inflamma- ground-glass opacity mainly distributing in the periphery
tory cells, alveolar collapse, and the increase of local of lung field or around the bronchial vascular bundle with
capillary blood volume. At this time, the patients were in the unclear boundary, which implies inflammatory exuda-
early course of disease, and the symptoms of patients were tion in alveolar cavity and alveolar septum in pathological.
mostly mild [2]. When the density of lung lesions increased, The CT findings show nodule (Fig.  2.1a, b), patchy shad-
it indicated that the course of disease was at an advanced ows (Fig. 2.1c–f). With the progression of disease, the focal
stage, the alveolar exudation increased more than before, lesion may develop into consolidation (Fig. 2.1g, h).
and some lesions merged with each other.
2. Consolidation. Consolidation refers to the replacement of
air in the alveoli by pathological fluids, cells, or tissues, 2.3 Consolidation
presented as the increase of pulmonary parenchymal den-
sity and multifocal, patchy, or segmental consolidation Consolidation refers to the alveolar air being replaced
shadows distributed in subpleural areas or along broncho- by pathological fluids, cells, or tissues, manifested by an
increase in pulmonary parenchymal density that obscures the
margins of underlying vessels and airway walls. Multifocal,
C. Yu (*) · W. Guan · S. Cai
patchy, or segmental consolidation are mainly distributed in
Guangzhou Eighth People’s Hospital, Guangzhou Medical
University, Guangzhou, China subpleural areas or along bronchovascular bundles.
Air bronchogram is a pattern of air-filled (tree branch-­
F. Shan
Shanghai Public Health Clinical Center, Fudan University, shape low-attenuation) bronchi on a background of pulmo-
Shanghai, China nary consolidation (Fig. 2.2a, b).

© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 9
J. Liu et al. (eds.), Atlas of Chest Imaging in COVID-19 Patients, https://doi.org/10.1007/978-981-16-1082-0_2
10 C. Yu et al.

a b

c d

e f

Fig. 2.1 (a) A 33-year-old male patient. CT scan shows two ground-­ lungs, with thickened vascular shadow (empty arrow). (e) A 63-year-­
glass nodules in the left lower lobe, with unclear boundary. (b) A old male patient. CT scan shows patchy ground-glass opacity in the left
26-year-old male patient. CT scan shows two ground-glass nodules in upper lobe, with unclear boundary and bronchiectasis. (f) Follow-up
the right lower lobe, with unclear boundary. (c) A 32-year-old female CT scans after 3 days; the lung involvement and density of lesion
patient. CT scan shows ground-glass opacity in the left lower lobe, with increased, with larger patchy ground-glass opacity and focal consolida-
thickened vascular shadow (empty arrow). (d) A 55-year-old female tion. (g, h) A 65-year-old male patient. CT scans show diffuse ground-­
patient. CT scan shows multiple ground-glass opacities in bilateral glass opacity in both lungs, with focal consolidation
2  Common CT Features of COVID-19 Pneumonia 11

g h

Fig. 2.1 (continued)

a b

Fig. 2.2 (a) A 39-year-old male patient. CT scan shows patchy consolidation in the left upper lobe, with “air bronchogram” sign inside (black
arrow). (b) A 43-year-old male patient. CT scan shows multiple ground-glass opacities and consolidation in bilateral lungs

2.4 Interstitial Changes Honeycomb-like shadow refers to a cystic translucent


shadow located in the center of the leaflet, demonstrating
1. Interlobular Septa and Lobular Interstitium Thickening “honeycomb” change, on the background of ground glass-­
like density shadow accompanied by thickened interlobular
Thickened interlobular septa can delineate the edge of the septal. On the formation basis, on the basis of “paving stone
lung lobule; when it is located on the periphery of the lung, sign,” the change of emphysema appears in the lobule center;
it often extends to the surface of the pleura, perpendicular to or on the basis of emphysema of the lobe center, a “paving
the pleural surface (Fig. 2.3a, b). Its appearance often sug- stone sign” appears (Fig. 2.3e, f).
gests interstitial exudation, cell infiltration, or fibrosis.
Crazy-paving sign demonstrates thickened interlobu- 2. Subpleural Curvilinear Line
lar septa and intralobular lines as a slight reticular pattern
with superimposition on a ground-glass opacity background, Subpleural curvilinear line is defined as a thin curvilinear
resembling irregular paving stone (Fig. 2.3c, d). opacity, lying less than 1 cm from and parallel to the pleu-
12 C. Yu et al.

a b

c d

e f

Fig. 2.3 (a) A 54-year-old male patient. CT scan shows multiple CT scan shows extensive ground-glass opacities in bilateral lungs, with
ground-glass opacities and stripe shadows in the bilateral lower lobes, peripheral and subpleural distribution; part of the lesion presents reticu-
and the thickened interlobular septa can be seen, which is obviously in lar pattern and “crazy-paving sign.” (e, f) A 62-year-old male patient.
the right lower lobe, perpendicular to the pleura (empty arrow). (b) A CT scans show multiple patchy ground-glass opacities in the lower
55-year-old female patient. An arc-shaped band of increased density lobes of both lungs. Increased grid-like density was observed in the
was seen in the lower lobe of the left lung adjacent to the dorsal pleura. lesion, with mixed small saccular lucent areas in it, resembling a
The interlobular septum in the lesion of the right lower lobe is thickened “honeycomb”-like change. (g–j) A 37-year-old male patient. (g) CT
and perpendicular to the pleura. (c) A 32-year-old female patient. CT scan shows subpleural curvilinear line in the bilateral lower lobes
scan shows ground-glass opacity in the left lower lobe, presenting retic- (empty arrow). The lesion gradually disappeared after 4 and 7 days of
ular pattern as “crazy-paving sign.” (d) A 55-year-old female patient. treatment (h)–(j)
2  Common CT Features of COVID-19 Pneumonia 13

g h

i j

Fig. 2.3 (continued)

ral surface, most commonly seen in the posterior of lower 2.6 Pleural Effusion
lobes, suggesting alveolar collapse or fibrosis. With effective
treatment, the subpleural curvilinear line of early stage could Pleural effusion is uncommon in patients with COVID-19
disappear gradually (Fig. 2.3g–j). pneumonia; some patients may have little pleural effusion
and pleural thickening (Fig. 2.5a, b).

2.5 Pleural Thickening


2.7 Halo Sign
The thickening of the pleura is the dense shadow of the band-­
like soft tissue along the chest wall, the thickness is uneven, The “halo sign” can be found in some nodules, sur-
the surface is not smooth, and the interface with the lung is rounded by ground-glass opacity, suggesting inflamma-
mostly visible with small adhesions. It is more common in tory exudation and edema of the alveolar compartment
COVID-19 pneumonia (Fig. 2.4a, b). (Fig. 2.6a, b).
14 C. Yu et al.

a b

Fig. 2.4 (a) A 56-year-old male patient. CT scan shows ground-glass patient. CT scan shows ground-glass opacities in both lungs with
opacity in both lungs, with unclear boundary. Some lesions were pulled unclear boundary. The thickened interlobular septum of the lesion and
near the pleura. The stripe shadow can be seen (empty arrow). The the “paving stone sign” can be seen. Some lesions were adjacent to
lesions are mainly distributed in the pleura. (b) A 56-year-old male pleural traction (empty arrow)

a b

Fig. 2.5 (a, b) A 71-year-old female patient. CT scans show multiple ground-glass opacities and reticular pattern, accompanied by pleural effusions

a b

Fig. 2.6 (a) A 33-year-old male patient. CT scan shows a nodule sur- multiple ground-glass opacities in bilateral lungs. A nodule of the left
rounded by ground-glass opacity in the right lower lobe, which mani- upper lobe is surrounded by ground-glass opacity and presents as “halo
fests as “halo sign.” (b) A 43-year-old male patient. CT scan shows sign” (empty arrow)
2  Common CT Features of COVID-19 Pneumonia 15

a b

c d

Fig. 2.7 (a–d) A 53-year-old male patient. CT scans show reversed CT scans on days 7, 13, and 18 of admission (b–d) show the decreased
halo signs in bilateral lower lobes (empty arrows) and focal rounded interior density of reversed halo sign in the right lower lobe. After effec-
ground-glass opacity with ring-like consolidation margin (a). Follow-up tive treatment, the lesions shrunk and disappeared gradually.

2. Chung M, Bernheim A, Mei X, et al. CT imaging features of 2019


2.8 Reversed Halo Sign novel coronavirus (2019-nCoV). Radiology. 2020;295(1):202–7.
https://doi.org/10.1148/radiol.2020200230.
Also called “atoll sign,” it is defined as a focal rounded 3. Hansell DM, Bankier AA, MacMahon H, McLoud TC, Müller
ground-glass opacity surrounded by annular or crescent-­ NL, Remy J.  Fleischner Society: glossary of terms for thoracic
­imaging. Radiology. 2008;246(3):697–722. https://doi.org/10.1148/
shaped consolidation. After effective treatment, the “reversed
radiol.2462070712.
halo sign” could disappear gradually (Fig. 2.7a–d). 4. Xu Z, Shi L, Wang Y, et  al. Pathological findings of COVID-­19
associated with acute respiratory distress syndrome [pub-
lished correction appears in Lancet Respir Med. 2020 Feb 25].
Lancet Respir Med. 2020;8(4):420–2. https://doi.org/10.1016/
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with 2019 novel coronavirus SARS-CoV-2. Eur J Nucl Med
Mol Imaging. 2020;47(5):1275–80. https://doi.org/10.1007/
s00259-­020-­04735-­9.
CT Features of Early COVID-19
Pneumonia (PCR-Positive) 3
Zhiping Zhang, Yan Ding, and Bihua Chen

3.1 Introduction and nonspecific and have significant overlap with those of
SARS and MERS.  In this chapter, we aim to describe the
Coronavirus disease (COVID-19) pneumonia is caused by early chest CT manifestations of COVID-19 to provide
severe acute respiratory syndrome coronavirus 2 (SARS-­ important reference values for early diagnosis, early preven-
CoV-­2) [1, 2]. It is highly infectious and spreads through tion, and early treatment of COVID-19 pneumonia.
respiratory droplets, contact, and the fecal-oral route. It is
characterized by acute onset and severe symptoms and is a
serious threat to human health and safety. According to the 3.2 Case 1 (Fig. 3.1a–l)
latest diagnosis and treatment scheme for COVID-19 pneu-
monia issued by the National Health Commission of the A 30-year-old male patient presented with fever for 3 days.
People’s Republic of China (trial version 8), the diagnosis of The body temperature peaked at 38  °C, accompanied by
COVID-19 pneumonia is mainly based on epidemiologic chills, cough, and throat discomfort, without expectoration.
factors, clinical manifestations, computed tomography (CT) He was exposed in the epidemic area. At admission, the body
findings, and nucleic acid detection of SARS-CoV-2. temperature was 36 °C, the pulse rate was 80 beats per min-
At the early stage of COVID-19 pneumonia, most lesions ute, the respiratory rate was 18 breaths per minute, and the
are multiple and distribute in the periphery of the lung or blood oxygen saturation was 98.2%. Blood routine examina-
subpleural regions, especially in the lower lobe of the lung. tion: white-cell count, lymphocyte count, and C-reactive
An investigation of initial chest CT imagings from 21 viral protein were 5.26  ×  109/L, 1.64  ×  109/L, and <10  mg/L,
RNA-confirmed COVID-19 patients found that 18 of 21 respectively.
(86%) patients had abnormal findings in the lung and the Chest CT scan taken 4 days after symptom onset showed
majority of them (16/18) had bilateral lung involvement [3]. multiple patchy ground-glass opacities in the lower lobe of
The common CT imaging features of COVID-19 pneumonia both lungs with blurred edge and “halo sign,” mainly located
include nodular or patchy ground-glass opacities with or in the peripheral area of the bilateral lung (Fig. 3.1a–l, white
without interlobular septal thickening and consolidative arrow). A ground-glass nodule was found in the posterior
opacities. Besides, halo sign, vascular thickening, crazy pav- basal segment of the left lower lobe (Fig.  3.1i, j, black
ing pattern, or air bronchogram sign was reported [4]. On the arrowhead).
contrary, pleural effusion, cavitation, and mediastinum and
hilar lymphadenopathy in COVID-19 are not commonly
detected. 3.3 Case 2 (Fig. 3.2a–l)
The clinical role of chest CT examination should be
emphasized. High-resolution CT is able to detect millimeter-­ A 29-year-old male patient presented with pharyngeal dis-
size lesions and plays an important role in the early diagnosis comfort, cough, and expectoration for 3 days. He was exposed
of viral pneumonia [5], including COVID-19 pneumonia [4, in the epidemic area. At admission, his body temperature was
6]. The reported imaging features in COVID-19 are variable 37.8 °C, the pulse rate was 97 beats per minute, the respira-
tory rate was 18 breaths per minute, and the blood oxygen
Z. Zhang (*) · Y. Ding · B. Chen
saturation was 96%. Blood routine examination: white-cell
Guangzhou Eighth People’s Hospital, Guangzhou Medical count, lymphocyte count, and C-reactive protein were
University, Guangzhou, China 5.25 × 109/L, 2.64 × 109/L, and <10 mg/L, respectively.

© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 17
J. Liu et al. (eds.), Atlas of Chest Imaging in COVID-19 Patients, https://doi.org/10.1007/978-981-16-1082-0_3
18 Z. Zhang et al.

a b

c d

e f

Fig. 3.1  Chest CT scan taken 4 days after symptom onset showed mul- the bilateral lung (a–l, white arrow). A ground-glass nodule was found
tiple patchy ground-glass opacities in the lower lobe of both lungs with in the posterior basal segment of the left lower lobe (i, j, black
blurred edge and “halo sign,” mainly located in the peripheral area of arrowhead)
3  CT Features of Early COVID-19 Pneumonia (PCR-Positive) 19

g h

i j

k l

Fig. 3.1 (continued)
20 Z. Zhang et al.

a b

c d

e f

Fig. 3.2  Chest CT scan taken 4 days after symptom onset showed multiple patchy ground-glass opacities in both lungs with blurring edge, mainly
distributed in the subpleural area of bilateral lower lobes (a–l)
3  CT Features of Early COVID-19 Pneumonia (PCR-Positive) 21

g h

i j

k l

Fig. 3.2 (continued)
22 Z. Zhang et al.

Chest CT scan taken 4 days after symptom onset showed 3.4 Case 3 (Fig. 3.3a–l)
multiple patchy ground-glass opacities in both lungs with
A 54-year-old female patient presented with fever for 3 days.
blurring edge, mainly distributed in the subpleural area of
The body temperature peaked at 38 °C, accompanied by dry
bilateral lower lobes (Fig. 3.2a–l).
cough, and she had the epidemiological history of exposure to

a b

c d

e f

Fig. 3.3  Chest CT examination performed 5 days after symptom onset demonstrated multifocal peripheral ground-glass opacities associated
showed multiple patchy ground-glass opacities in both lungs with blur- with intralobular septal thickening (a–h)
ring edge and subpleural distribution in the bilateral lower lobes. HRCT
3  CT Features of Early COVID-19 Pneumonia (PCR-Positive) 23

g h

i j

k l

Fig. 3.3 (continued)

patients from epidemic areas. At admission, her body tempera- gen saturation was 96.7%. Blood routine examination: white-
ture was 37  °C, the pulse rate was 93 beats per minute, the cell count, lymphocyte count, and C-reactive protein were
respiratory rate was 18 breaths per minute, and the blood oxy- 6.24 × 109/L, 2.18 × 109/L, and 25.68 mg/L, respectively.
24 Z. Zhang et al.

Chest CT examination performed 5 days after symptom 3.5 Case 4 (Fig. 3.4a–l)


onset showed multiple patchy ground-glass opacities in both
lungs with blurring edge and subpleural distribution in the A 45-year-old male patient presented with dry cough for 3
bilateral lower lobes. High-resolution computed tomography days without fever and chills, and he had the epidemiological
(HRCT) demonstrated multifocal peripheral ground-glass history of exposure to patients from epidemic areas. At
opacities associated with intralobular septal thickening admission, the body temperature was 36.8 °C, the pulse rate
(Fig. 3.3a–h). was 90 beats per minute, the respiratory rate was 18 breaths

a b

c d

e f

Fig. 3.4  Chest CT examination performed 3 days after symptom onset showed multiple patchy ground-glass opacities in the lower lobe of both
lungs with blurring edge, and the lesions were mainly distributed along the bronchovascular bundle (a–l)
3  CT Features of Early COVID-19 Pneumonia (PCR-Positive) 25

g h

i j

k l

Fig. 3.4 (continued)

per minute, and the blood oxygen saturation was 97.2%. Chest CT examination performed 3 days after symptom onset
Blood routine examination: white-cell count, lymphocyte showed multiple patchy ground-glass opacities in the lower lobe
count, and C-reactive protein were 9.05 × 109/L, 2.06 × 109/L, of both lungs with blurring edge, and the lesions were mainly
and <10 mg/L, respectively. distributed along the bronchovascular bundle (Fig. 3.4a–l).
26 Z. Zhang et al.

3.6 Case 5 (Fig. 3.5a–l) to patients from epidemic areas. At admission, the body tem-
perature was 37.8 °C, the pulse rate was 95 beats per minute,
A 32-year-old male patient presented with fever for 2 days, the respiratory rate was 20 breaths per minute, and the blood
without chills and shivering. His body temperature peaked at oxygen saturation was 98.5%. Blood routine examination:
38.2 °C before admission, accompanied by fatigue and chest white-cell count, lymphocyte count, and C-reactive protein
tightness, and he had the epidemiological history of exposure were 4.87 × 109/L, 2.11 × 109/L, and <10 mg/L, respectively.

a b

c d

e f

Fig. 3.5  Chest CT scan taken 3 days after symptom onset showed mul- observed in the lesions in the lateral basal segment of the left lower lobe
tiple patchy ground-glass opacities with blurring edge located in the (e–h), and subpleural curvilinear line appeared adjacent to the lesion in
subpleural area of the right middle lobe and the left lower lobe, espe- the posterior basal segment of the left lower lobe (i)
cially in the left lower lobe (a–l). Thickened blood vessel shadows were
3  CT Features of Early COVID-19 Pneumonia (PCR-Positive) 27

g h

i j

k l

Fig. 3.5 (continued)
28 Z. Zhang et al.

Chest CT scan taken 3 days after symptom onset showed 3.7 Case 6 (Fig. 3.6a–l)
multiple patchy ground-glass opacities with blurring edge
located in the subpleural area of the right middle lobe and the A 40-year-old male patient presented with fever for 3 days,
left lower lobe, especially in the left lower lobe (Fig. 3.5a–l). with no chills and shivering, and he had the epidemiological
Thickened blood vessel shadows were observed in the history of exposure to patients from epidemic areas. His
lesions in the lateral basal segment of the left lower lobe body temperature peaked at 38.4  °C before admission. At
(Fig. 3.5e–h), and subpleural curvilinear line appeared adja- admission, his body temperature was 37.2 °C, the pulse rate
cent to the lesion in the posterior basal segment of the left was 94 beats per minute, the respiratory rate was 18 breaths
lower lobe (Fig. 3.5i). per minute, and the blood oxygen saturation was 97.9%.

a b

c d

e f

Fig. 3.6  Chest CT scan taken 4 days after symptom onset showed multiple patchy ground-glass opacities in both lungs with blurring edge (a–l),
and subpleural curvilinear line and irregular linear opacities occurred in the bilateral lower lobes (e–j)
3  CT Features of Early COVID-19 Pneumonia (PCR-Positive) 29

g h

i j

k l

Fig. 3.6 (continued)

Blood routine examination: white-cell count, lymphocyte blurring edge (Fig.  3.6a–l), and subpleural curvilinear line
count, and C-reactive protein were 8.18 × 109/L, 1.24 × 109/L, and irregular linear opacities occurred in the bilateral lower
and 30.84 mg/L, respectively. lobes (Fig. 3.6e–j).
Chest CT scan taken 4 days after symptom onset showed
multiple patchy ground-glass opacities in both lungs with
30 Z. Zhang et al.

3.8 Case 7 (Fig. 3.7a–l) respiratory rate was 18 breaths per minute, and the blood
oxygen saturation was 97.6%. Blood routine examination:
A 26-year-old male patient was admitted to the hospital white-cell count, lymphocyte count, and C-reactive protein
because of 2 days of fever, accompanied by dry cough, and were 3.73  ×  109/L, 1.04  ×  109/L, and 45.40  mg/L,
he had the epidemiological history of exposure to patients respectively.
from epidemic areas. At admission, his body temperature Chest CT scan taken 2 days after symptom onset showed
was 38.5  °C, the pulse rate was 93 beats per minute, the multiple patchy ground-glass opacities in both lungs with blur-

a b

c d

e f

Fig. 3.7  Chest CT scan taken 2 days after symptom onset showed mul- lung (a–l). The central structure of lobules was thickened in the lesions
tiple patchy ground-glass opacities in both lungs with blurring edge, in the bilateral lower lobes, and locally thickened vascular shadows
and the lesions were mainly distributed in the subpleural area of the were found (c–j)
3  CT Features of Early COVID-19 Pneumonia (PCR-Positive) 31

g h

i j

k l

Fig. 3.7 (continued)

ring edge, and the lesions were mainly distributed in the subpleu- was thickened in the lesions in the bilateral lower lobes, and
ral area of the lung (Fig. 3.7a–l). The central structure of lobules locally thickened vascular shadows were found (Fig. 3.7c–j).
32 Z. Zhang et al.

3.9 Case 8 (Fig. 3.8a–l) 21 breaths per minute, and the blood oxygen saturation was
99%. Blood routine examination: white-cell count, lympho-
A 54-year-old female patient was admitted to the hospital cyte count, and C-reactive protein were 8.33  ×  109/L,
due to fever and fatigue for 2 days, accompanied by head- 2.65 × 109/L, and 15.11 mg/L, respectively.
ache and dry cough; the body temperature peaked at 37.7 °C, Chest CT examination performed 3 days after symp-
and she had a history of exposure to patients from epidemic tom onset showed multiple patchy ground-glass opacities
areas. At admission, the body temperature was 37.5 °C, the in both lungs with blurring edge; the lesions were mainly
pulse rate was 56 beats per minute, the respiratory rate was distributed in the superior segments of the bilateral lower

a b

c d

e f

Fig. 3.8  Chest CT examination performed 3 days after symptom onset ground-glass opacities associated with intralobular septal thickening,
showed multiple patchy ground-glass opacities in both lungs with blur- and a crazy-paving pattern can be seen (f–h). Besides, reversed halo
ring edge; the lesions were mainly distributed in the superior segments sign was observed in the lesion in the superior segment of the right
of the bilateral lower lobe (a–l). HRCT demonstrated multifocal lower lobe (d–g)
3  CT Features of Early COVID-19 Pneumonia (PCR-Positive) 33

g h

i j

k l

Fig. 3.8 (continued)

lobe (Fig.  3.8a–l). HRCT demonstrated multifocal (Fig. 3.8f–h). Besides, reversed halo sign was observed in
ground-glass opacities associated with intralobular septal the lesion in the superior segment of the right lower lobe
thickening, and a crazy-­ paving pattern can be seen (Fig. 3.8d–g).
34 Z. Zhang et al.

3.10 Case 9 (Fig. 3.9a–l) minute, the respiratory rate was 18 breaths per minute, and
the blood oxygen saturation was 97.1%. Blood routine
A 30-year-old female patient was admitted to the hospital examination: white-cell count, lymphocyte count, and
due to fever for 2 days; the body temperature peaked at C-reactive protein were 2.70  ×  109/L, 0.92  ×  109/L, and
38.7  °C, accompanied by chills and runny nose, with no <10 mg/L, respectively.
expectoration; she had the epidemiological history of expo- Chest CT examination performed 3 days after symp-
sure to patients from epidemic areas. At admission, the body tom onset showed patchy ground-glass opacities and con-
temperature was 38.2 °C, the pulse rate was 110 beats per solidation distributed in the subpleural area of the left

a b

c d

e f

Fig. 3.9  Chest CT examination performed 3 days after symptom onset ground-glass opacities associated with intralobular septal thickening,
showed patchy ground-glass opacities and consolidation distributed in and a crazy-paving pattern was observed (d, e, white arrow)
the subpleural area of the left lower lobe. HRCT demonstrated focal
3  CT Features of Early COVID-19 Pneumonia (PCR-Positive) 35

g h

i j

k l

Fig. 3.9 (continued)

lower lobe. HRCT demonstrated focal ground-glass opac- crazy-paving pattern was observed (Fig.  3.9d, e, white
ities associated with intralobular septal thickening, and a arrow).
36 Z. Zhang et al.

3.11 Case 10 (Fig. 3.10a–l) gen saturation was 97.1%. Blood routine examination:
white-cell count, lymphocyte count, and C-reactive pro-
A 65-year-old male patient was admitted to the hospital tein were 4.15  ×  109/L, 0.76  ×  109/L, and <10  mg/L,
because of dry cough and chills for 2 days, and he had the respectively.
epidemiological history of exposure to patients from epi- Chest CT examination performed 3 days after symptom
demic areas. At admission, the body temperature was onset showed multifocal ground-glass opacities mainly dis-
37.1 °C, the pulse rate was 103 beats per minute, the respi- tributed in the subpleural area of the bilateral lungs with
ratory rate was 20 breaths per minute, and the blood oxy- blurred edge (Fig.  3.10a–l). HRCT demonstrated focal

a b

c d

e f

Fig. 3.10  Chest CT examination performed 3 days after symptom septal thickening in the apicoposterior segment of the left upper lobe
onset showed multifocal ground-glass opacities mainly distributed in and the lateral segment of the right middle lobe, and a crazy-paving
the subpleural area of the bilateral lungs with blurred edge (a–l). HRCT pattern can be seen (a, e). Besides, the subpleural curvilinear line was
demonstrated focal ground-glass opacities associated with intralobular observed in the bilateral lower lobes (c–j)
3  CT Features of Early COVID-19 Pneumonia (PCR-Positive) 37

g h

i j

k l

Fig. 3.10 (continued)

ground-glass opacities associated with intralobular septal crazy-paving pattern can be seen (Fig. 3.10a, e). Besides, the
thickening in the apicoposterior segment of the left upper subpleural curvilinear line was observed in the bilateral
lobe and the lateral segment of the right middle lobe, and a lower lobes (Fig. 3.10c–j).
38 Z. Zhang et al.

3.12 Case 11 (Fig. 3.11a–l) gen saturation was 96%. Blood routine examination: white-
cell count, lymphocyte count, and C-reactive protein were
A 47-year-old female patient was admitted to the hospital due 4.68 × 109/L, 0.77 × 109/L, and 25.8 mg/L, respectively.
to fever for 3 days, accompanied by chills, cough, and expec- Chest CT examination performed 4 days after symptom
toration. She had the epidemiological history of exposure to onset showed multiple patchy ground-glass opacities mainly
patients from epidemic areas. At admission, the body tempera- distributed in the subpleural area of the bilateral lungs
ture was 38.5 °C, the pulse rate was 100 beats per minute, the (Fig. 3.11a–l). The subpleural curvilinear line was found in
respiratory rate was 20 breaths per minute, and the blood oxy- the bilateral lower lobes (Fig. 3.11e–j).

a b

c d

e f

Fig. 3.11  Chest CT examination performed 4 days after symptom onset showed multiple patchy ground-glass opacities mainly distributed in the
subpleural area of the bilateral lungs (a–l). The subpleural curvilinear line was found in the bilateral lower lobes (e–j)
3  CT Features of Early COVID-19 Pneumonia (PCR-Positive) 39

g h

i j

k l

Fig. 3.11 (continued)
40 Z. Zhang et al.

3.13 Case 12 (Fig. 3.12a–l) accompanied by chills, cough, and expectoration. He had the
epidemiological history of exposure to patients from epi-
A 27-year-old male patient was admitted to the hospital due demic areas. At admission, the body temperature was
to fever for 4 days; his body temperature peaked at 38.3 °C, 37.8 °C, the pulse rate was 105 beats per minute, the respira-

a b

c d

e f

Fig. 3.12  Chest CT examination performed 4 days after symptom lesions were predominantly found in the right lower lobe, with presence
onset showed multiple patchy ground-glass opacities mainly distributed of consolidation in which the “air bronchogram sign” could be seen
in the subpleural area of the bilateral lungs (a–l). Multifocal lung (e–h)
3  CT Features of Early COVID-19 Pneumonia (PCR-Positive) 41

g h

i j

k l

Fig. 3.12 (continued)
42 Z. Zhang et al.

tory rate was 20 breaths per minute, and the blood oxygen 3.14 Case 13 (Fig. 3.13a–l)
saturation was 97%. Blood routine examination: white-cell
count, lymphocyte count, and C-reactive protein were A 34-year-old male patient was admitted to the hospital due
3.34 × 109/L, 0.89 × 109/L, and 12.73 mg/L, respectively. to fever for 2 days; his body temperature peaked at 38.0 °C,
Chest CT examination performed 4 days after symptom accompanied by chills and cough, with no expectoration. He
onset showed multiple patchy ground-glass opacities mainly had the epidemiological history of exposure to patients from
distributed in the subpleural area of the bilateral lungs epidemic areas. At admission, the body temperature was
(Fig.  3.12a–l). Multifocal lung lesions were predominantly 37.5 °C, the pulse rate was 82 beats per minute, the respira-
found in the right lower lobe, with presence of consolidation in tory rate was 18 breaths per minute, and the blood oxygen
which the “air bronchogram sign” could be seen (Fig. 3.12e–h). saturation was 96%. Blood routine examination: white-cell

a b

c d

e f

Fig. 3.13  Chest CT examination performed 4 days after symptom onset showed multiple patchy ground-glass opacities in the bilateral lungs with
blurred edge and subpleural distribution (a–l). A few of lesions manifested as localized consolidation
3  CT Features of Early COVID-19 Pneumonia (PCR-Positive) 43

g h

i j

k l

Fig. 3.13 (continued)
44 Z. Zhang et al.

count, lymphocyte count, and C-reactive protein were 2. Chen N, Zhou M, Dong X, et al. Epidemiological and clinical char-
5.51 × 109/L, 0.99 × 109/L, and <10 mg/L, respectively. acteristics of 99 cases of 2019 novel coronavirus pneumonia in
Wuhan, China: a descriptive study. Lancet. 2020;395:507–13.
Chest CT examination performed 4 days after symptom 3. Chung M, Bernheim A, Mei X, et al. CT imaging features of 2019
onset showed multiple patchy ground-glass opacities in the novel coronavirus (2019-nCoV). Radiology. 2020;295:202–7.
bilateral lungs with blurred edge and subpleural distribution 4. Han R, Huang L, Dong J, et  al. Early clinical and CT manifesta-
tions of coronavirus disease 2019 (COVID-19) pneumonia. Am J
(Fig.  3.13a–l). A few of lesions manifested as localized
Roentgenol. 2020;215:338–43.
consolidation. 5. Paul NS, Roberts H, Butany J, et al. Radiologic pattern of disease in
patients with severe acute respiratory syndrome: the Toronto experi-
ence. RadioGraphics. 2004;24:553–63.
6. Holshue ML, DeBolt C, Lindquist S, et al. Washington State 2019-­
References nCoV Case Investigation Team. First case of 2019 novel coronavi-
rus in the United States. N Engl J Med. 2020;382:929–36.
1. Li Q, Guan X, Wu P, et al. Early transmission dynamics in Wuhan,
China, of novel coronavirus-infected pneumonia. N Engl J Med.
2020;382:1199–207.
CT Features of Intermediate Stage
of COVID-19 Pneumonia 4
Lin Lin, Xi Xu, and Weiping Cai

4.1 Introduction including increase in ground-glass opacity, consolidation,


and interstitial septal thickening. In another publication, Pan
The incubation period of COVID-19 ranges from 1 to 14 et al. [4] show enlarged lung involvement, increased ground-­
days after infection but is typically 3–7 days. Clinically, the glasses opacities, and consolidation in the follow-up CT scan
majority of patients in the intermediate stage of COVID-19 of 21 patients with confirmed COVID-19. Moreover, crazy-­
pneumonia develop deteriorated symptoms with noticeable paving sign was found on chest CT.
chest-computed tomography (CT) imaging changes. In con- Based on our observation, we summarize the chest CT
trast, a small proportion of patients only manifest mild or features of intermediate stage of COVID-19 pneumonia.
general symptoms, even when chest-CT imaging changes Most of patients enter the rapid disease-progression period
were easily observed. The mismatch between the develop- within 1 week after disease onset; only a few severe cases
ment of clinical symptoms and function changes of the lung progress rapidly within 2 weeks after disease onset. In the
detected by chest CT is probably because of the different early stage, chest CT manifests single or multiple ground-­
immune responses individually. Due to the advantages such glass opacity combined with thickening of intralobular or
as its fastness, high resolution, and direct visualization, chest interlobular septa in the unilateral or bilateral lung. As the
CT examination plays a critical role for precisely evaluat- disease progresses, the extent of lung involvement increases,
ing the patient conditions before initiating proper medical and the most common chest CT findings are ground-glass
treatment and for predicting the clinical outcome after treat- opacity with consolidation, interstitial septal thickening,
ment and thus was regarded as one of the vital references for and linear opacity. Sometimes, typical crazy-paving sign
COVID-19 diagnosis. can be seen. Other than that, some severe cases show bilat-
There are many publications on the chest CT findings eral diffuse patchy or massive consolidation with or without
during COVID-19 infection. Jin et al. [1] describe the fea- air-­bronchogram in follow-up chest CT.  However, lymph-
tures of chest CT in different disease courses, and they find adenopathy and pleural effusions can be found in few cases
large consolidative opacities and air bronchograms on chest with confirmed COVID-19. In the following case series, we
CT apart from ground-glass opacity during the progression present different chest CT findings of intermediate stage of
stage. Song et al. [2] report the increased rate of consolida- COVID-19 pneumonia in detail.
tion on chest CT with disease progression. Pan et al. [3], in
a retrospective study involving 63 patients with confirmed
COVID-19, demonstrate over 85% of patients having some 4.2 Case 1 (Fig. 4.1a1–e1, a2–e2)
features on chest CT associated with disease progression
A 30-year-old female patient with a disease-related exposure
history had fever, which occurred 2 days ago, accompanied
by chills and runny nose. Admission body temperature was
38.7  °C.  White blood cell count, lymphocyte count, and
L. Lin (*) · W. Cai C-reactive protein were 4.31  ×  109/L, 1.34  ×  109/L, and
Guangzhou Eighth People’s Hospital, Guangzhou Medical
University, Guangzhou, China <10  mg/L, respectively. The patient underwent chest CT
scans on day 3 and day 6 after the onset of symptoms and
X. Xu
The First Affiliated Hospital, Jinan University, Guangzhou, China was confirmed by CDC in Guangzhou.

© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 45
J. Liu et al. (eds.), Atlas of Chest Imaging in COVID-19 Patients, https://doi.org/10.1007/978-981-16-1082-0_4
46 L. Lin et al.

Chest CT scans on day 3 (a1–e1) showed patchy ground-­ and increased density of the lesions compared with previous
glass opacities with thickening of the interlobular and intra- images, indicating disease progression. Moreover, the inter-
lobular septa in the right upper lobe and left lower lobe. lobular septal thickening in regions of ground-glass opacifi-
Chest CT on day 6 (a2–e2) demonstrated enlarged lesions cation, represented a crazy-paving pattern.

a1 a2

b1 b2

c1 c2

Fig. 4.1  Chest CT scans on day 3 (a1–e1) showed patchy ground-glass compared with previous images, indicating disease progression.
opacities with thickening of the interlobular and intralobular septa in Moreover, the interlobular septal thickening in regions of ground-glass
the right upper lobe and left lower lobe. Chest CT on day 6 (a2–e2) opacification, represented a crazy-paving pattern
demonstrated enlarged lesions and increased density of the lesions
4  CT Features of Intermediate Stage of COVID-19 Pneumonia 47

d1 d2

e1 e2

Fig. 4.1 (continued)
48 L. Lin et al.

4.3 Case 2 (Fig. 4.2a1–e1, a2–e2) after the onset of symptoms and was confirmed by CDC in
Guangzhou.
A 65-year-old female patient with a disease-related Chest CT on day 3 (a1–e1) showed patchy ground-glass
exposure history presented with pharyngalgia for 1 day. opacities with thickened interlobular septa and intralobular
Admission body temperature was 36.7  °C.  White blood septa and focal consolidation in the bilateral lung. Chest CT
cell count, lymphocyte count, and C-reactive protein were on day 6 (a2–e2) demonstrated an enlargement of lesions
4.61  ×  109/L, 0.95  ×  109/L, and <10  mg/L, respectively. and increased consolidation. Most of lesions were located in
The patient underwent chest CT scans on day 3 and day 6 the peripheral field of the lung.

a1 a2

b1 b2

c1 c2

Fig. 4.2  Chest CT on day 3 (a1–e1) showed patchy ground-glass opac- strated an enlargement of lesions and increased consolidation. Most of
ities with thickened interlobular septa and intralobular septa and focal lesions were located in the peripheral field of the lung
consolidation in the bilateral lung. Chest CT on day 6 (a2–e2) demon-
4  CT Features of Intermediate Stage of COVID-19 Pneumonia 49

d1 d2

e1 e2

Fig. 4.2 (continued)
50 L. Lin et al.

4.4 Case 3 (Fig. 4.3a1–e1, a2–e2) went chest CT scans on day 13 and day 17 after the onset of
symptoms and was confirmed by CDC in Guangzhou.
A 63-year-old male patient presented with shortness of Chest CT on day 13 (a1–e1) showed diffuse ground-glass
breath for 10 days. Fever occurred 3 days ago, and admis- opacities with thickened interlobular septa and intralobular
sion body temperature was 37.8 °C. White blood cell count, septa, manifested as typical crazy-paving sign. Chest CT
lymphocyte count, and C-reactive protein were 6.70 × 109/L, on day 17 (a2–e2) demonstrated a significantly increase of
1.34 × 109/L, and 39.68 mg/L, respectively. The patient under- consolidation.

a1 a2

b1 b2

c1 c2

Fig. 4.3  Chest CT on day 13 (a1–e1) showed diffuse ground-glass opacities with thickened interlobular septa and intralobular septa, manifested
as typical crazy-paving sign. Chest CT on day 17 (a2–e2) demonstrated a significantly increase of consolidation
4  CT Features of Intermediate Stage of COVID-19 Pneumonia 51

d1 d2

e1 e2

Fig. 4.3 (continued)
52 L. Lin et al.

4.5 Case 4 (Fig. 4.4a1–e1, a2–e2) after the onset of symptoms and was confirmed by CDC in
Guangzhou.
A 37-year-old male patient with a disease-related expo- Chest CT on day 6 (a1–e1) showed multifocal ground-­glass
sure history had fever, which occurred 4 days ago, and opacities with interlobular and intralobular septal thickening
admission body temperature was 39.2  °C.  White blood and linear opacities in the bilateral lung, mainly in the periph-
cell count, lymphocyte count, and C-reactive protein were eral field of the lung. Typical crazy-paving sign (black arrow)
5.50  ×  109/L, 1.95  ×  109/L, and 34.59  mg/L, respectively. and subpleural linear opacity can be seen (white arrow). Chest
The patient underwent chest CT scans on day 6 and day 10 CT on day 10 (a2–e2) demonstrated the enlargement of lesions.

a1 a2

b1 b2

c1 c2

Fig. 4.4  Chest CT on day 6 (a1–e1) showed multifocal ground-glass Typical crazy-paving sign (black arrow) and subpleural linear opacity
opacities with interlobular and intralobular septal thickening and linear can be seen (white arrow). Chest CT on day 10 (a2–e2) demonstrated
opacities in the bilateral lung, mainly in the peripheral field of the lung. the enlargement of lesions
4  CT Features of Intermediate Stage of COVID-19 Pneumonia 53

d1 d2

e1 e2

Fig. 4.4 (continued)
54 L. Lin et al.

4.6 Case 5 (Fig. 4.5a1–e1, a2–e2) 16.77  mg/L, respectively. The patient underwent chest CT
scans on day 5 and day 9 after the onset of symptoms and
A 33-year-old male patient with a disease-related exposure was confirmed by CDC in Guangzhou.
history presented with runny nose for 3 days. Fever occurred Chest CT on day 5 (a1–e1) showed nodular and patchy
1 day ago, accompanied by cough. Admission body tempera- ground-glass opacities in the bilateral lung, mainly in the right
ture was 38.1 °C. White blood cell count, lymphocyte count, lower lobe. Chest CT on day 9 (a2–e2) demonstrated rapid pro-
and C-reactive protein were 5.46 × 109/L, 1.10 × 109/L, and gression of lesions with patchy consolidation and linear opacities.

a1 a2

b1 b2

c1 c2

Fig. 4.5  Chest CT on day 5 (a1–e1) showed nodular and patchy ground-glass opacities in the bilateral lung, mainly in the right lower lobe. Chest
CT on day 9 (a2–e2) demonstrated rapid progression of lesions with patchy consolidation and linear opacities
4  CT Features of Intermediate Stage of COVID-19 Pneumonia 55

d1 d2

e1 e2

Fig. 4.5 (continued)
56 L. Lin et al.

4.7 Case 6 (Fig. 4.6a1–e1, a2–e2) The patient underwent chest CT scans on day 5 and day 9
after the onset of symptoms and was confirmed by CDC
A 29-year-old male patient with a disease-related expo- in Guangzhou.
sure history presented with cough for 3 days. Admission Chest CT on day 5 (a1–e1) showed nodular and patchy
body temperature was 37.8  °C.  White blood cell ground-glass opacities in the bilateral lung. Chest CT on day
count, lymphocyte count, and C-reactive protein were 9 (a2–e2) demonstrated rapid progression of lesions with
7.93 × 109/L, 1.33 × 109/L, and 21.54 mg/L, respectively. patchy consolidation and thickened intralobular septa.

a1 a2

b1 b2

c1 c2

Fig. 4.6  Chest CT on day 5 (a1–e1) showed nodular and patchy ground-glass opacities in the bilateral lung. Chest CT on day 9 (a2–e2) demon-
strated rapid progression of lesions with patchy consolidation and thickened intralobular septa
4  CT Features of Intermediate Stage of COVID-19 Pneumonia 57

d1 d2

e1 e2

Fig. 4.6 (continued)
58 L. Lin et al.

4.8 Case 7 (Fig. 4.7a1–e1, a2–e2) The patient underwent chest CT scans on day 7 and day 11
after the onset of symptoms and was confirmed by CDC in
A 30-year-old male patient with a disease-related expo- Guangzhou.
sure history had fever, which occurred 4 days ago, Chest CT on day 7 (a1–e1) showed patchy consolidation
accompanied by cough, chills, myalgia, and headache. in the lower lobe of the bilateral lung. Chest CT on day 11
Admission body temperature was 39.1  °C.  White blood (a2–e2) demonstrated rapid progression of lesions with con-
cell count, lymphocyte count, and C-reactive protein were solidation, thickened interlobular septa, and subpleural lin-
5.25  ×  109/L, 2.64  ×  109/L, and <10  mg/L, respectively. ear opacity in the bilateral lung.

a1 a2

b1 b2

c1 c2

Fig. 4.7  Chest CT on day 7 (a1–e1) showed patchy consolidation in the lower lobe of the bilateral lung. Chest CT on day 11 (a2–e2) demonstrated
rapid progression of lesions with consolidation, thickened interlobular septa, and subpleural linear opacity in the bilateral lung
4  CT Features of Intermediate Stage of COVID-19 Pneumonia 59

d1 d2

e1 e2

Fig. 4.7 (continued)
60 L. Lin et al.

4.9 Case 8 (Fig. 4.8a1–e1, a2–e2) day 9 after the onset of symptoms and was confirmed by
CDC in Guangzhou.
A 50-year-old female patient with a disease-related exposure Chest CT on day 5 (a1–e1) showed nodular ground-
history presented with cough for 3 days. Fever occurred 1 day glass opacities with reversed halo sign in the right lung
ago, and admission body temperature was 38.0  °C.  White (white arrow). Chest CT on day 9 (a2–e2) demonstrated
blood cell count, lymphocyte count, and C-reactive protein the shrink of reversed halo sign, replaced by the enlarge-
were 4.35  ×  109/L, 1.44  ×  109/L, and 12.16  mg/L, respec- ment of lesions with consolidation and linear opacities in
tively. The patient underwent chest CT scans on day 5 and the bilateral lung.

a1 a2

b1 b2

c1 c2

Fig. 4.8  Chest CT on day 5 (a1–e1) showed nodular ground-glass replaced by the enlargement of lesions with consolidation and linear
opacities with reversed halo sign in the right lung (white arrow). Chest opacities in the bilateral lung
CT on day 9 (a2–e2) demonstrated the shrink of reversed halo sign,
4  CT Features of Intermediate Stage of COVID-19 Pneumonia 61

d1 d2

e1 e2

Fig. 4.8 (continued)
62 L. Lin et al.

4.10 Case 9 (Fig. 4.9a1–e1, a2–e2) The patient underwent chest CT scans on day 9 and day 12
after the onset of symptoms and was confirmed by CDC in
A 39-year-old female patient with a disease-related expo- Guangzhou.
sure history had fever, which occurred 1 day ago, and Chest CT on day 9 (a1–e1) showed patchy ground-glass
admission body temperature was 36.7  °C.  White blood opacities in the right lower lobe. Chest CT on day 12 (a2–e2)
cell count, lymphocyte count, and C-reactive protein were demonstrated the enlargement of lesions with intralobular
4.83  ×  109/L, 1.11  ×  109/L, and <10  mg/L, respectively. and interlobular septal thickening.

a1 a2

b1 b2

c1 c2

Fig. 4.9  Chest CT on day 9 (a1–e1) showed patchy ground-glass opacities in the right lower lobe. Chest CT on day 12 (a2–e2) demonstrated the
enlargement of lesions with intralobular and interlobular septal thickening
4  CT Features of Intermediate Stage of COVID-19 Pneumonia 63

d1 d2

e1 e2

Fig. 4.9 (continued)
64 L. Lin et al.

4.11 Case 10 (Fig. 4.10a1–e1, a2–e2) underwent chest CT scans on day 11 and day 15 after
the onset of symptoms and was confirmed by CDC in
A 70-year-old male patient with a disease-related exposure Guangzhou.
history had fever, which occurred 8 days ago, accompanied Chest CT on day 11 (a1–e1) showed diffuse patchy
by cough, chills, myalgia, and fatigue. Admission body ground-glass opacities with thickened intralobular and inter-
temperature was 37.8  °C.  White blood cell count, lym- lobular septa in the bilateral lung. Chest CT on day 15 (a2–
phocyte count, and C-reactive protein were 7.05  ×  109/L, e2) demonstrated the enlargement of lesions with typical
0.56  ×  109/L, and 92.82  mg/L, respectively. The patient crazy-paving sign and lobular consolidation.

a1 a2

b1 b2

c1 c2

Fig. 4.10  Chest CT on day 11 (a1–e1) showed diffuse patchy ground-glass opacities with thickened intralobular and interlobular septa in the
bilateral lung. Chest CT on day 15 (a2–e2) demonstrated the enlargement of lesions with typical crazy-paving sign and lobular consolidation
4  CT Features of Intermediate Stage of COVID-19 Pneumonia 65

d1 d2

e1 e2

Fig. 4.10 (continued)
66 L. Lin et al.

4.12 Case 11 (Fig. 4.11a1–e1, a2–e2) phocyte count, and C-reactive protein were 3.48  ×  109/L,
1.56  ×  109/L, and 25.68  mg/L, respectively. The patient
A 64-year-old female patient with a disease-related expo- underwent chest CT scans on day 10 and day 13 after
sure history presented with fever for 8 days. Admission the onset of symptoms and was confirmed by CDC in
body temperature was 38.2 °C. White blood cell count, lym- Guangzhou.

a1 a2

b1 b2

c1 c2

Fig. 4.11  Chest CT on day 10 (a1–e1) showed multifocal patchy ground-glass opacities in the bilateral lung. Chest CT on day 13 (a2–e2) dem-
onstrated the enlargement of lesions with lobular consolidation and linear opacities
4  CT Features of Intermediate Stage of COVID-19 Pneumonia 67

d1 d2

e1 e2

Fig. 4.11 (continued)
68 L. Lin et al.

Chest CT on day 10 (a1–e1) showed multifocal patchy 4.13 Case 12 (Fig. 4.12a1–e1, a2–e2)
ground-glass opacities in the bilateral lung. Chest CT on day
13 (a2–e2) demonstrated the enlargement of lesions with A 58-year-old male patient with a disease-related exposure
lobular consolidation and linear opacities. history presented with cough for 7 days. Fever occurred 1 day
ago, and admission body temperature was 38.5  °C.  White

a1 a2

b1 b2

c1 c2

Fig. 4.12  Chest CT on day 10 (a1–e1) showed multifocal patchy ground-glass opacities with thickened interlobular septa and lobular consolida-
tion in the bilateral lung. Chest CT on day 15 (a2–e2) demonstrated the enlargement of lesions with patchy consolidation
4  CT Features of Intermediate Stage of COVID-19 Pneumonia 69

d1 d2

e1 e2

Fig. 4.12 (continued)
70 L. Lin et al.

blood cell count, lymphocyte count, and C-reactive protein 2. Song F, Shi N, Shan F, et  al. Emerging coronavirus 2019-nCoV
were 2.61  ×  109/L, 0.53  ×  109/L, and 74.43  mg/L, respec- pneumonia. Radiology. 2020;295(1):210–7. https://doi.org/10.1148/
radiol.2020200274. Epub 2020 Feb 6
tively. The patient underwent chest CT scans on day 10 and 3. Pan Y, Guan H, Zhou S, et  al. Initial CT findings and temporal
day 15 after the onset of symptoms and was confirmed by changes in patients with the novel coronavirus pneumonia (2019-­
CDC in Guangzhou. nCoV): a study of 63 patients in Wuhan, China. Eur Radiol.
2020;30(6):3306–9. https://doi.org/10.1007/s00330-­020-­06731-­x.
Chest CT on day 10 (a1–e1) showed multifocal patchy
Epub 2020 Feb 13
ground-glass opacities with thickened interlobular septa and 4. Pan F, Ye T, Sun P, et al. Time course of lung changes on chest CT
lobular consolidation in the bilateral lung. Chest CT on day during recovery from 2019 novel coronavirus (COVID-19) pneu-
15 (a2–e2) demonstrated the enlargement of lesions with monia. Radiology. 2020;295(3):715–21. https://doi.org/10.1148/
radiol.2020200370. Epub 2020 Feb 13
patchy consolidation.

References
1. Jin YH, Cai L, Cheng ZS, et  al. A rapid advice guideline for the
diagnosis and treatment of 2019 novel coronavirus (2019-nCoV)
infected pneumonia (standard version). Mil Med Res. 2020;7(1):4.
https://doi.org/10.1186/s40779-­020-­0233-­6.
CT Features of Late Stage of COVID-19
Pneumonia 5
Yanhong Yang, Peixu Wang, and Fengjuan Chen

5.1 Introduction ness of breath. She had no exposure to an infected patient


or epidemic area. The body temperature at admission was
In the late stage of COVID-19 pneumonia, the patients’ clin- 38.4  °C.  White blood cell count, neutrophil count, lym-
ical symptoms improved as the lung lesions gradually disap- phocyte count, and C-reactive protein were 7.56  ×  109/L,
peared. After approximately 14 days, the absorption of lung 5.98  ×  109/L, 1.21  ×  109/L, and 95.96  mg/L, respectively.
lesions on chest computed tomography (CT) was reported The patient was laboratory confirmed by novel coronavirus
in 75% of the patients, and the imaging features included nucleic acid throat swab test in Guangzhou CDC. Chest CT
decreased number of involved lobes, reduction of crazy-­ examination was performed 12 days and 22 days after the
paving pattern, and consolidative opacities [1]. onset of symptoms.
According to the database collected from the patients admit- On day 12 after the onset of symptoms, chest CT images
ted to Guangzhou Eighth People’s Hospital, we found that the (Fig.  5.1a1–e1) showed that patchy ground-glass opacities
absorption time of the lesions on chest-CT imaging was later with thickening of the interlobular septa were found in the
than that of the improvement of clinical symptoms or negative bilateral lung, representing a crazy-paving pattern (Fig. 5.1a1,
conversion of viral RNA and the imaging features associated white arrow), with focal consolidation. After oxygen ther-
with clinical improvement usually occur after 2 weeks of onset apy, anti-infection and anti-asthmatic therapy, phlegm elimi-
[2–4]. Chest-CT findings in late stage usually showed a reduc- nation, treatment with traditional Chinese medicine, and
tion in the size and density of lung lesions. Most of the lung other treatment, the body temperature returned to normal
lesions can be gradually absorbed and can disappear. for 1 week, the symptoms of the patient were improved sig-
Chest-CT imaging showed that inflammation absorption nificantly, and the real-time fluorescence polymerase chain
was one of the indicators to evaluate whether patients can be reaction of the patient’s pharyngeal swab was negative for
discharged from the hospital. The image recommendations two consecutive times of COVID-19 nucleic acid. On day 22
for patients meeting discharge standards are the following: after the onset of symptoms, chest CT images (Fig. 5.1a2–
(1) The scope of the lesions in the lung is significantly e2) showed most of the lesions in the bilateral lung decreased
reduced (the volume of the lesion is reduced by 50% and the and disappeared, compared with previous images, but a few
density is reduced by 50%); most of it is absorbed or com- linear opacities remained, compared with previous images
pletely dissipated. (Fig. 5.1e2).
(2) Only a few linear opacities remain in the lungs.
(3) No new lesions are detected in the lungs.
5.3 Case 2 (Fig. 5.2a1–e1, a2–e2)

5.2 Case 1 (Fig. 5.1a1–e1, a2–e2) A 36-year-old male with fever for 9 days, accompanied by
aggravated rash, dry cough, and limb joint muscle sore-
A 58-year-old woman was admitted to the hospital with ness for 1 day, was admitted, and he was exposed to con-
repeated cough and expectoration for 12 days and fever firmed cases with novel coronavirus pneumonia. The body
for 9 days, accompanied by chest tightness and short- ­temperature at admission was 39.1  °C.  White blood cell
count, neutrophil count, lymphocyte count, and C-reactive
protein were 3.74 × 109/L, 1.59 × 109/L, 1.64 × 109/L, and
Y. Yang (*) · P. Wang · F. Chen
Guangzhou Eighth People’s Hospital, Guangzhou Medical <10  mg/L, respectively. The patient was laboratory con-
University, Guangzhou, China firmed by novel coronavirus nucleic acid throat swab test in

© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 71
J. Liu et al. (eds.), Atlas of Chest Imaging in COVID-19 Patients, https://doi.org/10.1007/978-981-16-1082-0_5
72 Y. Yang et al.

a1 a2

b1 b2

c1 c2

Fig. 5.1  On day 12 after the onset of symptoms, chest CT images symptoms of the patient were improved significantly, and the real-­time
(a1–e1) showed that patchy ground-glass opacities with thickening of fluorescence polymerase chain reaction of the patient’s pharyngeal
the interlobular septa were found in the bilateral lung, representing a swab was negative for two consecutive times of COVID-19 nucleic
crazy-paving pattern (a1 white arrow), with focal consolidation. After acid. On day 22 after the onset of symptoms, chest CT images (a2–e2)
oxygen therapy, anti-infection and anti-asthmatic therapy, phlegm elim- showed most of the lesions in the bilateral lung decreased and disap-
ination, treatment with traditional Chinese medicine, and other treat- peared, compared with previous images, but a few linear opacities
ments, the body temperature returned to normal for 1 week, the remained, compared with previous images (e2)

Guangzhou CDC. Chest CT examination was performed 10 ties were found in the bilateral lung. After antiviral, anti-­
days and 21 days after the onset of symptoms (Fig. 5.2a1–e1, infection, and anti-asthmatic therapy, phlegm elimination,
a2–e2). and treatment with traditional Chinese medicine, the body
On day 10 after the onset of symptoms, chest CT images temperature returned to normal for 10 days, the clinical
(Fig.  5.2a1–e1) showed that patchy ground-glass opaci- symptoms of the patient were improved significantly, and
5  CT Features of Late Stage of COVID-19 Pneumonia 73

d1 d2

e1 e2

Fig. 5.1 (continued)

the real-time fluorescence polymerase chain reaction of the of symptoms, chest CT images (Fig. 5.2a2–e2) demonstrated
patient’s pharyngeal swab was negative for two consecutive most of the lesions in the bilateral lung decreased and disap-
times of COVID-19 nucleic acid. On day 21 after the onset peared, compared with previous images.
74 Y. Yang et al.

a1 a2

b1 b2

c1 c2

Fig. 5.2  On day 10 after the onset of symptoms, chest CT images rescence polymerase chain reaction of the patient’s pharyngeal swab
(a1–e1) showed that patchy ground-glass opacities were found in the was negative for two consecutive times of COVID-19 nucleic acid. On
bilateral lung. After antiviral, anti-infection, and anti-asthmatic therapy, day 21 after the onset of symptoms, chest CT images (a2–e2) demon-
phlegm elimination, and treatment with traditional Chinese medicine, strated most of the lesions in the bilateral lung decreased and disap-
the body temperature returned to normal for 10 days, the clinical symp- peared, compared with previous images
toms of the patient were improved significantly, and the real-time fluo-
5  CT Features of Late Stage of COVID-19 Pneumonia 75

d1 d2

e1 e2

Fig. 5.2 (continued)

5.4 Case 3 (Fig. 5.3a1–e1, a2–e2) respectively. The patient was laboratory confirmed by novel
coronavirus nucleic acid throat swab test in Guangzhou
A 35-year-old male with fever for 2 days, accompanied by CDC.  Chest CT examination was performed 5 days and 20
cough and expectoration, was admitted, and he was exposed to days after the onset of symptoms (Fig. 5.3a1–e1, a2–e2).
confirmed cases with novel coronavirus pneumonia. The body On day 5 after the onset of symptoms, chest CT images
temperature at admission was 39.1 °C. White blood cell count, (Fig.  5.3a1–e1) showed that patchy ground-glass opaci-
neutrophil count, lymphocyte count, and C-reactive protein ties were found in the bilateral lung, accompanied by
were 5.62 × 109/L, 1.31 × 109/L, 0.3 × 109/L, and 18.04 mg/L, partial consolidation and linear opacities. After antiviral
76 Y. Yang et al.

a1 a2

b1 b2

c1 c2

Fig. 5.3  On day 5 after the onset of symptoms, chest CT images (a1– cantly, and the real-time fluorescence polymerase chain reaction of the
e1) showed that patchy ground-glass opacities were found in the bilat- patient’s pharyngeal swab was negative for two consecutive times of
eral lung, accompanied by partial consolidation and linear opacities. COVID-19 nucleic acid. On day 20 after the onset of symptoms, chest
After antiviral and anti-infection therapy and treatment with traditional CT images (a2–e2) demonstrated most of the lesions in the bilateral
Chinese medicine, the body temperature returned to normal for 2 lung decreased and disappeared, but a few linear opacities remained,
weeks, the clinical symptoms of the patient were improved signifi- compared with previous images (c2)

and anti-­infection therapy and treatment with traditional improved significantly, and the real-time fluorescence
Chinese medicine, the body temperature returned to nor- polymerase chain reaction of the patient’s pharyngeal
mal for 2 weeks, the clinical symptoms of the patient were swab was negative for two consecutive times of COVID-
5  CT Features of Late Stage of COVID-19 Pneumonia 77

d1 d2

e1 e2

Fig. 5.3 (continued)
78 Y. Yang et al.

19 nucleic acid. On day 20 after the onset of symptoms, 5.5 Case 4 (Fig. 5.4a1–e1, a2–e2)
chest CT images (Fig. 5.3a2–e2) demonstrated most of the
lesions in the bilateral lung decreased and disappeared, A 28-year-old male with cough, phlegm, and fatigue for 8
but a few linear opacities remained, compared with previ- days and fever for 3 days was admitted. He had no exposure
ous images (Fig. 5.3c2). to an infected patient or epidemic area. The body tempera-

a1 a2

b1 b2

c1 c2

Fig. 5.4  On day 8 after the onset of symptoms, chest CT images (a1– symptoms of the patient were improved significantly, and the real-time
e1) showed that patchy ground-glass opacities with thickening of the fluorescence polymerase chain reaction of the patient’s pharyngeal
interlobular septa were found in the bilateral lung, representing a crazy-­ swab was negative for two consecutive times of COVID-19 nucleic
paving pattern. The body temperature returned to normal the next day acid. On day 26 after the onset of symptoms, chest CT images (a2–e2)
after admission, after “oxygen therapy, anti-infection therapy, phlegm demonstrated the lesions in the bilateral lung decreased, compared with
elimination, cough relieving, and immune enhancement”; the clinical previous images
5  CT Features of Late Stage of COVID-19 Pneumonia 79

d1 d2

e1 e2

Fig. 5.4 (continued)
80 Y. Yang et al.

ture at admission was 39.6 °C. White blood cell count, neu- 38.5 °C. White blood cell count, neutrophil count, lym-
trophil count, lymphocyte count, and C-reactive protein were phocyte count, and C-reactive protein were 3.76 × 109/L,
2.20 × 109/L, 1.48 × 109/L, 0.64 × 109/L, and 46.63 mg/L, 1.71  ×  109/L, 1.71  ×  109/L, and 22.48  mg/L, respec-
respectively. The patient was laboratory confirmed by novel tively. The patient was laboratory confirmed by novel
coronavirus nucleic acid throat swab test in Guangzhou coronavirus nucleic acid throat swab test in Guangzhou
CDC. Chest CT examination was performed 8 days and 26 CDC. Chest CT examination was performed 7 days and
days after the onset of symptoms (Fig. 5.4a1–e1, a2–e2). 20 days after the onset of symptoms (Fig.  5.5a1–e1,
On day 8 after the onset of symptoms, chest CT a2–e2).
images (Fig. 5.4a1–e1) showed that patchy ground-glass On day 7 after the onset of symptoms, chest CT images
opacities with thickening of the interlobular septa were (Fig. 5.5a1–e1) showed that patchy ground-glass opacities
found in the bilateral lung, representing a crazy-paving with thickening of the interlobular septa and linear opaci-
pattern. The body temperature returned to normal the ties were found in the bilateral lung, mainly distributed
next day after admission, after “oxygen therapy, anti- under the pleura. After antiviral and anti-infection ther-
infection therapy, phlegm elimination, cough relieving, apy, phlegm elimination, cough relieving, and treatment
and immune enhancement”; the clinical symptoms of the with traditional Chinese medicine, the body temperature
patient were improved significantly, and the real-time returned to normal the next day after admission, the clini-
fluorescence polymerase chain reaction of the patient’s cal symptoms improved significantly, and the real-time
pharyngeal swab was negative for two consecutive times fluorescence polymerase chain reaction of the patient’s
of COVID-19 nucleic acid. On day 26 after the onset pharyngeal swab was negative for two consecutive times
of symptoms, chest CT images (Fig.  5.4a2–e2) demon- of COVID-19 nucleic acid. On day 20 after the onset of
strated the lesions in the bilateral lung decreased, com- symptoms, chest CT images (Fig. 5.5a2–e2) demonstrated
pared with previous images. the lesions in the bilateral lung decreased and disappeared,
compared with previous images.

5.6 Case 5 (Fig. 5.5a1–e1, a2–e2)

A 48-year-old male with fever for 1 week was admitted.


He was exposed to confirmed cases with novel coronavi-
rus pneumonia. The body temperature at admission was
5  CT Features of Late Stage of COVID-19 Pneumonia 81

a1 a2

b1 b2

c1 c2

d1 d2

Fig. 5.5  On day 7 after the onset of symptoms, chest CT images (a1– next day after admission, the clinical symptoms improved significantly,
e1) showed that patchy ground glass opacities with thickening of the and the real-time fluorescence polymerase chain reaction of the patient’s
interlobular septa and linear opacities were found in the bilateral lung, pharyngeal swab was negative for two consecutive times of COVID-19
mainly distributed under the pleura. After antiviral and anti-infection nucleic acid. On day 20 after the onset of symptoms, chest CT images
therapy, phlegm elimination, cough relieving, and treatment with tradi- (a2–e2) demonstrated the lesions in the bilateral lung decreased and
tional Chinese medicine, the body temperature returned to normal the disappeared, compared with previous images
82 Y. Yang et al.

e1 e2

Fig. 5.5 (continued)

5.7 Case 6 (Fig. 5.6a1–e1, a2–e2) On day 7 after the onset of symptoms, chest CT images
(Fig.  5.6a1–e1) showed that patchy ground-glass opaci-
A 37-year-old female with fever for 7 days and diarrhea and ties in the bilateral lung were mainly distributed under the
chest tightness for 3 days was admitted. She was exposed pleura, accompanied by partial consolidation (Fig. 5.6c1),
to confirmed cases with novel coronavirus pneumonia. and subpleural curvilinear line was found in the bilateral
The body temperature at admission was 38.2  °C.  White lung (Fig.  5.6a1). After oxygen therapy and antiviral and
blood cell count, neutrophil count, lymphocyte count, anti-­infection therapy, the body temperature returned to
and C-reactive protein were 6.31  ×  109/L, 4.93  ×  109/L, normal for 7 days, the clinical symptoms of the patient
1.07  ×  109/L, and 57.32  mg/L, respectively. The patient were improved significantly, and the real-time fluorescence
was laboratory confirmed by novel coronavirus nucleic polymerase chain reaction of the patient’s pharyngeal swab
acid throat swab test in Guangzhou CDC. Chest CT exam- was negative for two consecutive times of COVID-19
ination was performed 7 days and 14 days after the onset nucleic acid. On day 14 after the onset of symptoms, chest
of symptoms (Fig. 5.6a1–e1, a2–e2). CT images (Fig. 5.6a2–e2) demonstrated the lesions in the
bilateral lung decreased, compared with previous images.
5  CT Features of Late Stage of COVID-19 Pneumonia 83

a1 a2

b1 b1

c1 c2

Fig. 5.6  On day 7 after the onset of symptoms, chest CT images (a1– of the patient were improved significantly, and the real-time fluores-
e1) showed that patchy ground glass opacities in the bilateral lung were cence polymerase chain reaction of the patient’s pharyngeal swab was
mainly distributed under the pleura, accompanied by partial consolida- negative for two consecutive times of COVID-19 nucleic acid. On day
tion (c1), and subpleural curvilinear line was found in the bilateral lung 14 after the onset of symptoms, chest CT images (a2–e2) demonstrated
(a1). After oxygen therapy and antiviral and anti-infection therapy, the the lesions in the bilateral lung decreased, compared with previous
body temperature returned to normal for 7 days, the clinical symptoms images
84 Y. Yang et al.

d1 d2

e1 e2

Fig. 5.6 (continued)

5.8 Case 7 (Fig. 5.7a1–e1, a2–e2) tein were 4.13  ×  109/L, 2.42  ×  109/L, 1.33  ×  109/L, and
51.12 mg/L, respectively. The patient was laboratory con-
A 30-year-old male with fever and cough for 4 days, firmed by novel coronavirus nucleic acid throat swab test in
accompanied by chills, muscle soreness, dizziness, and Guangzhou CDC. Chest CT examination was performed 4
poor appetite, was admitted. He was exposed to confirmed days and 15 days after the onset of symptoms (Fig. 5.7a1–
cases with novel coronavirus pneumonia. The body tem- e1, a2–e2).
perature at admission was 39.1 °C. White blood cell count, On day 4 after the onset of symptoms, chest CT images
neutrophil count, lymphocyte count, and C-reactive pro- (Fig.  5.7a1–e1) showed that patchy consolidation was
5  CT Features of Late Stage of COVID-19 Pneumonia 85

a1 a2

b1 b2

c1 c2

Fig. 5.7  On day 4 after the onset of symptoms, chest CT images (a1– chain reaction of the patient’s pharyngeal swab was negative for two
e1) showed that patchy consolidation was found in the bilateral lung, consecutive times of COVID-19 nucleic acid. On day 15 after the onset
with air bronchogram signs. After antiviral, anti-infection, and anti-­ of symptoms, chest CT images (a2–e2) demonstrated most of the
inflammatory therapy and reinforcing immunity, the body temperature lesions in the bilateral lung disappeared, but a few linear opacities
returned to normal for 9 days, the clinical symptoms of the patient were remained, compared with previous images
improved significantly, and the real-time fluorescence polymerase

found in the bilateral lung, with air bronchogram signs. pharyngeal swab was negative for two consecutive times
After antiviral, anti-infection, and anti-inflammatory of COVID-19 nucleic acid. On day 15 after the onset of
therapy and reinforcing immunity, the body temperature symptoms, chest CT images (Fig. 5.7a2–e2) demonstrated
returned to normal for 9 days, the clinical symptoms of most of the lesions in the bilateral lung disappeared, but
the patient were improved significantly, and the real-time a few linear opacities remained, compared with previous
fluorescence polymerase chain reaction of the patient’s images.
86 Y. Yang et al.

d1 d2

e1 e2

Fig. 5.7 (continued)
5  CT Features of Late Stage of COVID-19 Pneumonia 87

5.9 Case 8 (Fig. 5.8a1–e1, a2–e2) 2.60 × 109/L, 0.8 × 109/L, and<10 mg/L, respectively. The


patient was laboratory confirmed by novel coronavirus
A 33-year-old male was admitted with fever and cough nucleic acid throat swab test in Guangzhou CDC. Chest CT
for 5 days. He was exposed to confirmed cases with novel examination was performed 7 days and 20 days after the
coronavirus pneumonia. The body temperature at admis- onset of symptoms (Fig. 5.8a1–e1, a2–e2).
sion was 37.9 °C. White blood cell count, neutrophil count, On day 7 after the onset of symptoms, chest CT images
lymphocyte count, and C-reactive protein were 3.73 × 109/L, (Fig.  5.8a1–e1) showed that patchy ground-glass opacities

a1 a2

b1 b2

c1 c2

Fig. 5.8  On day 7 after the onset of symptoms, chest CT images (a1– cence polymerase chain reaction of the patient’s pharyngeal swab was
e1) showed that patchy ground-glass opacities with thickening of the negative for two consecutive times of COVID-19 nucleic acid. On day
interlobular septa were found in the bilateral lung, accompanied by par- 20 after the onset of symptoms, chest CT images (a2–e2) demonstrated
tial consolidation (c1). After antiviral and anti-­infection therapy, the the lesions in the bilateral lung decreased, compared with previous
body temperature returned to normal for 7 days, the clinical symptoms images
of the patient were improved significantly, and the real-time fluores-
88 Y. Yang et al.

d1 d2

e1 e2

Fig. 5.8 (continued)

with thickening of the interlobular septa were found in the toms of the patient were improved significantly, and the real-
bilateral lung, accompanied by partial consolidation (Fig. time fluorescence polymerase chain reaction of the patient’s
5.8c1). After antiviral and anti-infection therapy, the body pharyngeal swab was negative for two consecutive times of
temperature returned to normal for 7 days, the clinical symp- COVID-19 nucleic acid. On day 20 after the onset of symp-
5  CT Features of Late Stage of COVID-19 Pneumonia 89

toms, chest CT images (Fig.  5.8a2–e2) demonstrated the 2. Das KM, Lee EY, Al Jawder SE, et al. Acute Middle East respira-
tory syndrome coronavirus: temporal lung changes observed on the
lesions in the bilateral lung decreased, compared with previ- chest radiographs of 55 patients. AJR. 2015:W267–74. [web]
ous images. 3. Müller NL, Ooi GC, Khong PL, et  al. High-resolution CT find-
ings of severe acute respiratory syndrome at presentation and after
admission. AJR. 2004;182:39–44.
4. Ooi GC, Khong PL, Müller NL, et al. Severe acute respiratory syn-
References drome: temporal lung changes at thin-section CT in 30 patients.
Radiology. 2004;230:836–44.
1. Pan F, Ye T, Sun P, et al. Time course of lung changes on chest CT
during recovery from 2019 novel coronavirus (COVID-19) pneu-
monia. Radiology. 2020; [Epub ahead of print]
Chest Features of Severe and Critical
Patients with COVID-19 Pneumonia 6
Jing Qu, Xilong Deng, and Yanqing Ding

6.1 Introduction 1. Multiple ground-glass opacities and consolidative opaci-


ties in bilateral lungs.
In some COVID-19 patients, the disease progresses rapidly, 2. The thickened vascular profile can be seen in ground-
resulting in respiratory failure, multiple organ dysfunction or glass opacities, and “air bronchi signs” may be present,
failure, and even death sometimes. which can be accompanied by bronchiectasis.
According to the novel coronavirus pneumonia treatment 3. Interlobular septum and subpleural interstitium thickening
strategies [1]: is common. In severe cases, most of the bilateral lung may
be affected, presenting as “white lung”-like or “white lung.”
1. Any one of the following conditions is considered as 4. A small amount of pleural effusion can be seen in very
severe type: few patients [2–4].
(a) Respiratory distress, RR ≥ 30 times/min. 3. Individuals at increased risk of severe and critical
(b) At rest, oxygen saturation ≤93%. illness

(c) Arterial partial oxygen pressure (PaO2)/oxygen (a) People over 65
absorption concentration (FiO2) ≤300 mmHg. (b) People with cardiovascular and cerebrovascular dis-
(d) Chest images showed significant progression of
eases (including hypertension), chronic lung diseases
lesions more than 50% within 24–48 h. (chronic obstructive pulmonary disease, moderate to
2. Any of the following conditions are considered as critical severe asthma), diabetes, chronic liver and kidney
type: diseases, tumors, and other basic diseases
(a) Respiratory failure, requiring mechanical ventilation. (c) People with immunodeficiencies (e.g., in AIDS
(b) Shock. patients, long-term use of corticosteroids or other
(c) Patients with other organ failure should be treated in immunosuppressive drugs)
the intensive care unit (ICU). (d) Obese people (body mass index ≥30)
(e) Women in the third trimester of pregnancy and peri-
This chapter aims to improve the understanding of chest natal period
imaging features in severe and critical COVID-19 by pre- (f) Heavy smokers
senting clinical characteristics and dynamic chest CT images 4. Prognostic factors for deteriorated conditions
of relevant cases. (a) Adults
Chest CT imaging features of severe and critical cases:
If one or a combination of the following signs shows up,
the COVID-19 patients should be closely monitored and
pre-­treated in cases of disease deterioration: (1) progressive
aggravation of hypoxemia or respiratory distress; (2) tissue
J. Qu (*) · X. Deng
Guangzhou Eighth People’s Hospital, Guangzhou Medical oxygenation index deteriorates or lactic acid increases pro-
University, Guangzhou, China gressively; (3) peripheral blood lymphocyte count reduces
Y. Ding progressively or peripheral blood inflammatory markers
Nanfang Hospital, Southern Medical University, Guangzhou, such as IL-6, CRP, and ferritin are progressively increased;
China (4) indexes related to coagulation function, such as D-dimer,

© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 91
J. Liu et al. (eds.), Atlas of Chest Imaging in COVID-19 Patients, https://doi.org/10.1007/978-981-16-1082-0_6
92 J. Qu et al.

increases significantly; (5) chest images show significant at admission was 38.6 °C, and the highest temperature in the
progression of pulmonary lesions. course of the disease was 39  °C.  Laboratory examination:
white blood cell count in peripheral blood was 4.58 × 109/L,
(b) Children the lymphocyte count was 1.05 × 109/L, the C-reactive protein
• Increased respiratory rate. was 30.75 mg/L, and the oxygenation index was 245 mmHg.
• Poor mental reaction and lethargy. The patient was laboratory confirmed by novel coronavirus
• Progressive increase of lactic acid. nucleic acid throat swab test in Guangzhou CDC. Chest CT
• Inflammatory markers such as CRP, PCT, and ferritin examination was performed on day 2 (8 days after the onset
are significantly increased. of symptoms), day 7 (13 days after the onset of symptoms),
• Chest CT images demonstrate bilateral and multiple and day 14 of admission (20 days after the onset of symp-
opacities, pleural effusion, or rapid progression of toms) (Fig. 6.1a–l).
lesions in a short period. On day 2 of admission, chest CT images showed multiple
• Underlying diseases (congenital heart disease, bron- ground-glass opacities in the bilateral lungs, with subpleural
chopulmonary dysplasia, respiratory malformations, distribution (Fig. 6.1a–d).
abnormal hemoglobin, severe malnutrition, etc.), On day 7 of admission, after anti-infection and anti-
immunodeficiency (long-term use of immunosup- pyretic treatment, low-flow oxygen inhalation through a
pressive agents), or hypoxia and neonates. nasal catheter, and other treatments, the patient had heavier
symptoms than before. Chest CT images showed increased
density of multiple lesions and thickened interlobular septum
6.2 Case 1 (Fig. 6.1a–l) (Fig. 6.1e–h).
On day 14 of admission, after anti-infection therapy and
A 60-year-old woman was admitted to the hospital with maintenance of electrolyte acid-base balance, the patient’s
repeated fever and cough for 7 days. She had no exposure to condition was further aggravated. Chest CT images showed
an infected patient or epidemic area. The body temperature increased and enlarged lesions of bilateral lungs (Fig. 6.1i–l).
6  Chest Features of Severe and Critical Patients with COVID-19 Pneumonia 93

a b

c d

e f

Fig. 6.1  On day 2 of admission, chest CT images showed multiple CT images showed increased density of multiple lesions and thickened
ground-glass opacities in the bilateral lungs, with subpleural distribu- interlobular septum (e–h). On day 14 of admission, after anti-infection
tion (a–d). On day 7 of admission, after anti-infection and antipyretic treatment and maintenance of electrolyte acid-base balance, the
treatment, low-flow oxygen inhalation through a nasal catheter, and patient’s condition was further aggravated. Chest CT images showed
other treatments, the patient had heavier symptoms than before. Chest increased and enlarged lesions of bilateral lungs (i–l)
94 J. Qu et al.

g h

i j

k l

Fig. 6.1 (continued)

6.3 Case 2 (Fig. 6.2a–l) admission was 37.9  °C.  Laboratory examination: white
blood cell count in peripheral blood was 4.26 × 109/L, the
A 59-year-old male got a fever for 4 days, and he was lymphocyte count was 1.36  ×  109/L, and the C-reactive
exposed in the epidemic area. The body temperature at protein was 12.33 mg/L. The patient was laboratory con-
6  Chest Features of Severe and Critical Patients with COVID-19 Pneumonia 95

a b

c d

e f

Fig. 6.2  On day 4 of admission, chest CT images showed multiple sion, the patient underwent anti-infection and antivirus treatment,
ground-glass opacities and consolidations in subpleural regions of both immunity enhancement, and high-frequency humidification-assisted
lungs (a–d). On day 6 of admission, after high-frequency humidification-­ ventilation treatment; subsequently, his symptoms improved signifi-
assisted ventilation and anti-infection, anti-inflammatory, and nutri- cantly. The range of multifocal lesions was reduced. However, the local
tional support treatment, the patient’s symptoms did not improve density increased, the interlobular septum was thickened, and the sub-
significantly. Chest CT images showed increased density of multiple pleural line (hollow arrow) was present (i–l)
lesions and thickened interlobular septum (e–h). On day 16 of admis-
96 J. Qu et al.

g h

i j

k l

Fig. 6.2 (continued)

firmed by novel coronavirus nucleic acid throat swab test days after the onset of symptoms), and day 16 of admis-
in Guangzhou CDC. Chest CT examination was performed sion (19 days after the onset of symptoms), as shown in
on day 4 (7 days after the onset of symptoms), day 6 (9 Fig. 6.2a–l.
6  Chest Features of Severe and Critical Patients with COVID-19 Pneumonia 97

On day 4 of admission, chest CT images showed mul- 37.9  °C, and the highest temperature in the course of the
tiple ground-glass opacities and consolidations in subpleural disease was 39  °C.  Laboratory examination: white blood
regions of both lungs (Fig. 6.2a–d). cell count in peripheral blood was 8.91 × 109/L, the lym-
On day 6 of admission, after high-frequency phocyte count was 0.48 × 109/L, the C-reactive protein was
humidification-­assisted ventilation and anti-infection, anti-­ 50.27 mg/L, and the D-dimer was 1870 μg/L. The patient
inflammatory, and nutritional support treatment, the patient’s was laboratory confirmed by novel coronavirus nucleic
symptoms did not improve significantly. Chest CT images acid throat swab test in Guangzhou CDC. Chest CT exami-
showed increased density of multiple lesions and thickened nation was performed on day 2, day 7, and day 15 of admis-
interlobular septum (Fig. 6.2e–h). sion (19 days after the onset of symptoms), as shown in
On day 16 of admission, the patient underwent anti-­ Fig. 6.3a–l.
infection and antivirus treatment, immunity enhancement, and On day 2 of admission, CT images exhibited multiple
high-frequency humidification-assisted ventilation treatment; ground-glass opacities in the right upper lobe. The inter-
subsequently, his symptoms improved significantly. The range lobular septum and the right oblique fissure were thickened
of multifocal lesions was reduced. However, the local density (Fig. 6.3a–d).
increased, the interlobular septum was thickened, and the sub- On day 7 of admission, after high-frequency humidifi-
pleural line (hollow arrow) was present (Fig. 6.2i–l). cation and antiviral therapy, the clinical symptoms of the
patient improved. Chest CT images showed reduced lesions,
but the local density was increased (Fig. 6.3e–h).
6.4 Case 3 (Fig. 6.3a–l) On day 15 of admission, after high-frequency humidi-
fication and antiviral therapy, the clinical symptoms of the
A 62-year-old male was admitted with fever, cough, and patients improved. CT scan showed decreased lesions, com-
expectoration for more than 10 days. He was exposed in pared with previous images (Fig. 6.3i–l).
the epidemic area. The body temperature at admission was
98 J. Qu et al.

a b

c d

e f

Fig. 6.3  On day 2 of admission, CT images exhibited multiple ground-­ but the local density was increased (e–h). On day 15 of admission, after
glass opacities in the right upper lobe. The interlobular septum and the high-frequency humidification and antiviral therapy, the clinical symp-
right oblique fissure were thickened (a–d). On day 7 of admission, after toms of the patients improved. CT scan showed decreased lesions, com-
high-frequency humidification and antiviral therapy, the clinical symp- pared with previous images (i–l)
toms of the patient improved. Chest CT images showed reduced lesions,
6  Chest Features of Severe and Critical Patients with COVID-19 Pneumonia 99

g h

i j

k l

Fig. 6.3 (continued)

6.5 Case 4 (Fig. 6.4a–j) 37.7 °C. Laboratory examination: white blood cell count in


peripheral blood was 11.5  ×  109/L, the lymphocyte count
A 72-year-old male was admitted to the hospital for 5 days, was 0.89 × 109/L, the C-reactive protein was 34.2 mg/L, and
and he was exposed to suspected cases with novel corona- the D-dimer was 1520 μg/L. The patient was laboratory con-
virus pneumonia. His body temperature at admission was firmed by novel coronavirus nucleic acid throat swab test in
100 J. Qu et al.

a b

c d

e f

Fig. 6.4  On day 2 of admission, CT images showed ground-glass treatment, the symptoms were aggravated. Chest CT images showed
opacities in the subpleural regions of the left upper lobe (a–d). On day new multiple ground-glass opacities and consolidation in the upper and
7 of admission, after high-flow oxygen therapy, combined anti-­ lower lobes of both lungs. The volume of the upper left lobe reduced
infection, anti-inflammatory, and anti-shock therapy, and symptomatic (e–j)

Guangzhou CDC. Chest CT examination was performed on On day 7 of admission, after high-flow oxygen therapy,
day 2 and day 7 of admission, as shown in Fig. 6.4a–j. combined anti-infection, anti-inflammatory, and anti-shock
On day 2 of admission, CT images showed ground-glass therapy, and symptomatic treatment, the symptoms were
opacities in the subpleural regions of the left upper lobe aggravated. Chest CT images showed new multiple ground-­
(Fig. 6.4a–d). glass opacities and consolidation in the upper and lower
6  Chest Features of Severe and Critical Patients with COVID-19 Pneumonia 101

g h

j
i

Fig. 6.4 (continued)

lobes of both lungs. The volume of the upper left lobe


On day 3 of admission, chest CT images showed ground-­
reduced (Fig. 6.4e–j).
glass opacities in subpleural regions of bilateral lungs
(Fig. 6.5a–d).
On day 6 of admission, the patient was treated with a low-­
6.6 Case 5 (Fig. 6.5a–l) flow nasal catheter for oxygen inhalation and anti-infection,
anti-inflammatory, and immune-enhancing treatment. The
A 58-year-old male was admitted to the hospital for 9 symptoms of the patient were aggravated. Chest CT images
days, and he was exposed to suspected cases with novel showed increased and enlarged lesions of both lungs, the
coronavirus pneumonia. The body temperature at admis- interlobular septum thickened, and the subpleural line was
sion was 38 °C. Laboratory examination: white blood cell present. (Fig. 6.5e–h).
count in peripheral blood was 6.69 × 109/L, the lympho- On day 9 of admission, the patient was transferred to
cyte count was 2.14  ×  109/L, and the C-reactive protein the ICU. After treatment with high-flow humidified oxygen
was 25.1  mg/L.  The patient was laboratory confirmed therapy instrument-assisted breathing and adjustment of
by novel coronavirus nucleic acid throat swab test in anti-­infection strategy, the condition was further aggravated.
Guangzhou CDC. Chest CT examination was performed Chest CT images showed that the lung lesions increased and
on day 3, day 6, and day 9 of admission, as shown in enlarged, and the intralobular septa and interlobular septa
Fig. 6.5a–l. thickening were more obviously than before (Fig. 6.5i–l).
102 J. Qu et al.

a b

c d

e f

Fig. 6.5  On day 3 of admission, chest CT images showed ground-glass (e–h). On day 9 of admission, the patient was transferred to the
opacities in subpleural regions of bilateral lungs (a–d). On day 6 of ICU.  After treatment with high-flow humidified oxygen therapy
admission, the patient was treated with a low-flow nasal catheter for instrument-­assisted breathing and adjustment of anti-infection strategy,
oxygen inhalation and anti-infection, anti-inflammatory, and immune-­ the condition was further aggravated. Chest CT images showed that the
enhancing treatment. The symptoms of the patient were aggravated. lung lesions increased and enlarged, and the intralobular septa and
Chest CT images showed increased and enlarged lesions of both lungs, interlobular septa thickening were more obviously than before (i–l)
the interlobular septum thickened, and the subpleural line was present
6  Chest Features of Severe and Critical Patients with COVID-19 Pneumonia 103

g h

i j

k l

Fig. 6.5 (continued)

6.7 Case 6 (Fig. 6.6a–l) perature in the course of the disease was 38.4 °C. Laboratory
examination: white blood cell count in peripheral blood was
A 61-year-old female was admitted to the hospital with 4.29  ×  109/L, the lymphocyte count was 1.07  ×  109/L, the
cough and sputum for 11 days and fever for 2 days. The body C-reactive protein was 63.66  mg/L, and the D-dimer was
temperature at admission was 36.5 °C, and the highest tem- 1460 μg/L. The patient was laboratory confirmed by novel
104 J. Qu et al.

a b

c d

e f

Fig. 6.6  On day 1 of admission, chest CT scan showed ground-glass the bilateral lobes (e–h). On day 12 of admission, after anti-infection,
opacities, partial consolidation, and local interlobular septal thickening anti-inflammation, and high-to-medium-flow oxygen therapy, the
in the bilateral lungs (a–d). On day 5 of admission, after anti-infection patient’s symptoms improved. Chest CT scan showed decreased multi-
and medium-flow oxygen therapy, the symptoms were worse than ple lung lesions and thickening of the interlobular septum (i–l)
before. Chest CT scan showed increased and enlarged lung lesions in

coronavirus nucleic acid throat swab test in Guangzhou On day 1 of admission, chest CT scan showed ground-­
CDC.  Chest CT examination was performed on day 1 (5 glass opacities, partial consolidation, and local interlobular
days after the onset of symptoms), day 5 (9 days after the septal thickening in the bilateral lungs (Fig. 6.6a–d).
onset of symptoms), and day 12 (16 days after the onset of On day 5 of admission, after anti-infection and medium-­
symptoms) of admission, as shown in Fig. 6.6a–l. flow oxygen therapy, the symptoms were worse than before.
6  Chest Features of Severe and Critical Patients with COVID-19 Pneumonia 105

g h

i j

k l

Fig. 6.6 (continued)

Chest CT scan showed increased and enlarged lung lesions 6.8 Case 7 (Fig. 6.7a–l)
in the bilateral lobes (Fig. 6.6e–h).
On day 12 of admission, after anti-infection, anti-­ A 61-year-old female was admitted to the hospital with
inflammation, and high-to-medium-flow oxygen therapy, cough and sputum for 11 days and fever for 2 days.
the patient’s symptoms improved. Chest CT scan showed The body temperature at admission was 36.5  °C, and
decreased multiple lung lesions and thickening of the inter- the highest t­emperature in the course of the disease was
lobular septum (Fig. 6.6i–l). 38.4 °C. Laboratory examination: white blood cell count in
106 J. Qu et al.

a b

c d

e f

Fig. 6.7  On day 2 of admission, chest CT scan showed multiple symptoms improved. Chest CT scan showed decreased lesions in the
ground-glass opacities, partial consolidation, and local interlobular sep- bilateral lungs (e–h). On day 17 of admission, the patient underwent the
tal thickening in the bilateral lungs (a–d). On day 8 of admission, after same treatment as before, and the symptoms turned better than before.
high-frequency humidification-assisted ventilation and anti-infection, The chest CT images showed that the bilateral lung lesions decreased,
anti-fungus, anti-inflammatory, and antivirus treatment, the patient’s compared with previous images (i–l)
6  Chest Features of Severe and Critical Patients with COVID-19 Pneumonia 107

g h

i j

k l

Fig. 6.7 (continued)
108 J. Qu et al.

peripheral blood was 4.29 × 109/L, the lymphocyte count was peripheral blood was 4.39 × 109/L, the lymphocyte count was
1.07  ×  109/L, the C-reactive protein was 63.66  mg/L, and 0.47 × 109/L, and the C-reactive protein was 108.8 mg/L. The
the D-dimer was 1460 μg/L. The patient was laboratory con- patient was laboratory confirmed by novel coronavirus
firmed by novel coronavirus nucleic acid throat swab test in nucleic acid throat swab test in Guangzhou CDC. Chest CT
Guangzhou CDC. Chest CT examination was performed on examination was performed on day 4 (15 days after the onset
day 2 (13 days after the onset of symptoms), day 8 (19 days of symptoms) and day 12 (23 days after the onset of symp-
after the onset of symptoms), and day 17 (28 days after the toms). Bedside chest radiographs were taken on day 16 (27
onset of symptoms) of admission, as shown in Fig. 6.7a–l. days after the onset of symptoms), day 18 (29 days after the
On day 2 of admission, chest CT scan showed multiple onset of symptoms), and day 24 (35 days after the onset of
ground-glass opacities, partial consolidation, and local inter- symptoms), shown in Fig. 6.8a–k.
lobular septal thickening in the bilateral lungs (Fig. 6.7a–d). On day 4 of admission, chest CT images showed exten-
On day 8 of admission, after high-frequency sive ground-glass opacities and consolidation (with air
humidification-­ assisted ventilation and anti-infection, bronchogram sign) of bilateral lungs and thickening of the
anti-­
fungus, anti-inflammatory, and antivirus treatment, interlobular septa, forming a “crazy-paving pattern” (hollow
the patient’s symptoms improved. Chest CT scan showed arrow), and subpleural subline was present (Fig. 6.8a–d).
decreased lesions in the bilateral lungs (Fig. 6.7e–h). On day 12 of admission, after assisted ventilation and
On day 17 of admission, the patient underwent the anti-infection treatment, the symptoms of the patients were
same treatment as before, and the symptoms turned better worse than before. Chest CT scan showed the increased den-
than before. The chest CT images showed that the bilateral sity of bilateral lung lesions (Fig. 6.8e–h).
lung lesions decreased, compared with previous images On day 16 of admission, bedside chest radiograph of the
(Fig. 6.7i–l). patient showed multiple ground-glass opacities in bilateral
lungs, especially in the lower lobes (Fig. 6.8i).
On day 18 of admission, the patient’s symptoms were
6.9 Case 8 (Fig. 6.8a–k) worse than before, and the reexamination of the bedside
chest radiograph showed enlarged lesions and progressive
A 65-year-old male was admitted to the hospital with fever ground-glass opacities in both lower lobes, indicating dis-
for 11 days, diarrhea for 5 days, and shortness of breath for ease progression (Fig. 6.8j).
3 days. The body temperature at admission was 37.5  °C, On day 24 of admission, the patient’s symptoms improved,
and the highest temperature in the course of the disease was and the bedside chest radiograph showed that lesions were
39.2 °C. Laboratory examination: white blood cell count in reduced (Fig. 6.8k).
6  Chest Features of Severe and Critical Patients with COVID-19 Pneumonia 109

a b

c d

e f

Fig. 6.8  On day 4 of admission, chest CT images showed extensive patient showed multiple ground-glass opacities in bilateral lungs, espe-
ground-glass opacities and consolidation (with air bronchogram sign) cially in the lower lobes (i). On day 18 of admission, the patient’s symp-
of bilateral lungs and thickening of the interlobular septa, forming a toms were worse than before, and the reexamination of the bedside
“crazy-paving pattern” (hollow arrow), and subpleural subline was chest radiograph showed enlarged lesions and progressive ground-glass
present (a–d). On day 12 of admission, after assisted ventilation and opacities in both lower lobes, indicating disease progression (j). On day
anti-infection treatment, the symptoms of the patients were worse than 24 of admission, the patient’s symptoms improved, and the bedside
before. Chest CT scan showed the increased density of bilateral lung chest radiograph showed that lesions were reduced (k)
lesions (e–h). On day 16 of admission, bedside chest radiograph of the
110 J. Qu et al.

g h

i j

Fig. 6.8 (continued)
6  Chest Features of Severe and Critical Patients with COVID-19 Pneumonia 111

6.10 Case 9 (Fig. 6.9a–k) On day 6 of admission, the patient was admitted to ICU
after high-flow mask oxygen inhalation and antiviral, anti-­
A 55-year-old female was admitted to the hospital with infection, and anti-inflammatory treatment, and the symp-
fever for 2 days. The body temperature at admission was toms were more severe than before. Chest CT images showed
38  °C, and the highest temperature in the course of the that the bilateral lung lesions increased and enlarged, with
disease was 38.1 °C. Laboratory examination: white blood the range increased by more than 50%, and the interlobular
cell count in peripheral blood was 6.29 × 109/L, the lym- septum thickened; “crazy-paving pattern” (hollow arrow)
phocyte count was 2.09 × 109/L, the C-reactive protein was was observed (Fig. 6.9e–h).
20.37 mg/L, and the D-dimer was 1090 μg/L. The patient On day 9 of admission, the patient’s symptoms were aggra-
was laboratory confirmed by novel coronavirus nucleic vated; bedside chest radiograph of the patient showed mul-
acid throat swab test in Guangzhou CDC. Chest CT exami- tiple ground-glass opacities in the bilateral lungs (Fig. 6.9i).
nation was performed on day 1 (3 days after the onset of On day 14 of admission, the patient’s symptoms
symptoms) and day 6 (8 days after the onset of symptoms). improved, and the bedside chest radiograph showed pro-
Bedside chest radiographs were taken on day 9 (11 days gressive lesions in both lower lobes compared with previous
after the onset of symptoms), day 14 (16 days after the images (Fig. 6.9j).
onset of symptoms), and day 17 (19 days after the onset of On day 17 of admission, the patient’s symptoms did not
symptoms), shown in Fig. 6.9a–k. improve significantly, and the bedside chest radiograph
On day 1 of admission, chest CT scan showed ground-­ showed that lesions were more aggravated than before, and
glass opacities in multiple lobes (Fig. 6.9a–d). the bilateral lung showed like “white lung” (Fig. 6.9k).
112 J. Qu et al.

a b

c d

e f

Fig. 6.9  On day 1 of admission, chest CT scan showed ground-glass sion, the patient’s symptoms were aggravated; bedside chest radiograph
opacities in multiple lobes (a–d). On day 6 of admission, the patient of the patient showed multiple ground-glass opacities in the bilateral
was admitted to ICU after high-flow mask oxygen inhalation and anti- lungs (i). On day 14 of admission, the patient’s symptoms improved,
viral, anti-infection, and anti-inflammatory treatment, and the symp- and the bedside chest radiograph showed progressive lesions in both
toms were more severe than before. Chest CT images showed that the lower lobes compared with previous images (j). On day 17 of admis-
bilateral lung lesions increased and enlarged, with the range increased sion, the patient’s symptoms did not improve significantly, and the bed-
by more than 50%, and the interlobular septum thickened; a “crazy-­ side chest radiograph showed that lesions were more aggravated than
paving pattern” (hollow arrow) was observed (e–h). On day 9 of admis- before, and the bilateral lung showed like “white lung” (k)
6  Chest Features of Severe and Critical Patients with COVID-19 Pneumonia 113

g h

i j

Fig. 6.9 (continued)
114 J. Qu et al.

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syndrome coronavirus: what does a radiologist need to know? AJR
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1. Huang C, Wang Y, Li X, et al. Clinical features of patients infected with
AJR.15.15363.
2019 novel coronavirus in Wuhan, China. Lancet. 2020;395:497–
4. Chung M, Bernheim A, Mei X, et al. CT imaging features of 2019
506. https://doi.org/10.1016/S0140-­6736(20)30183-­5.
novel coronavirus (2019-nCoV). Radiology. 2020; https://doi.
2.
Ooi GC, Daqing M.  SARS: radiological features.
org/10.1148/radiol.2020200230.
Respirology. 2003;8(Suppl):S15–9. https://doi.org/10.1046/
j.1440-1843.2003.00519.x.
Role of CT and CT Features of Suspected
COVID-19 Patients (PCR Negative) 7
Qingxin Gan, Tianli Hu, and Songfeng Jiang

7.1 Introduction For most of suspected patients, the common features on


chest CT are single or multiple, nodular or patchy ground-­glass
The COVID-19 pneumonia is a specific infectious disease opacities with or without blurred margin; most of the lesions
caused by severe acute respiratory syndrome coronavirus 2 are located in the peripheral region of the lung, especially in
(SARS-COV-2) which is a single-stranded positive-strand the lower lobes. In few cases, chest CT images show patchy
RNA virus and has not been found in humans previously [1– ground-glass opacities in the bilateral lung with focal consolida-
3]. Since the outbreak of COVID-19 in January 2020, it has tion shadows. In this chapter, we aim to describe the CT features
spread rapidly among general population through respiratory of suspected COVID-19 pneumonia patients with negative find-
droplets and indirect or direct contact, especially in middle- ing of PCR to improve the detection rate of the disease in detail.
aged and elderly people [4–6]. The incubation period of
COVID-19 pneumonia is 1–14 days, usually 3–7 days. The
main clinical manifestations are fever, fatigue, dry cough, 7.2 Case 1 (Fig. 7.1a–j)
and muscle soreness, a few accompanied by nasal conges-
tion, runny nose, diarrhea, and so on [7]. Most patients pres- A 64-year-old female patient, who had no exposure to epi-
ent with mild clinical symptoms initially, while for some demic areas. On January 20, 2020, she went out for dinner
severe or critically ill patients, symptoms can manifest as with her family. The next day, she developed fever with a
dyspnea and hypoxemia within a week and progress to respi- temperature of up to 38.5 °C, accompanied by headache and
ratory failure and death [8, 9]. body aches, with no aversion to cold or shivering, no cough-
At present, the detection of SARS-CoV-2 viral RNA by ing or expectoration, and no tightness or shortness of breath.
RT-PCR is the gold standard for confirmation of COVID- On January 21, 2020, CT examination was performed, and
19. Unfortunately, the rate of detectable viral RNA in the chest CT images showed pneumonia. The clinical symp-
upper respiratory swab samples is only 30–50%, which toms did not significantly improve after 1 week of treatment.
is much lower than 76.4% of CT [10]. The main reason Body temperature fluctuated from 37.5  °C to 38.5  °C.  At
is that virus is not detectable in nasal and pharynx swabs the time of admission, the body temperature was 38.2  °C,
even when virus replicates in the lung. At this time, the the respiratory rate was 18 breaths per minute, total white
suspected patients should have chest CT examination to blood cell count was 3.48  ×  109/L, C-reactive protein was
exclude the infection of COVID-19 pneumonia. If the 25.68 mg/L, neutrophil count was 1.50 × 109/L, lymphocyte
chest CT images of suspected patient show evidence of count was 1.56 × 109/L, platelet count was 134 × 109/L, and
progressive COVID-19 pneumonia, they should be admit- oxygen saturation was 97.5%. The viral RNA in throat swab
ted to the hospital for isolation and treatment immediately was negative for three examinations. In her fourth exami-
and take multiple nucleic acid tests for subsequent con- nation, she was finally confirmed by Guangzhou CDC. On
firmation. Therefore, diagnosis of COVID-19 pneumonia January 30, 2020, chest CT images showed multiple patchy
should be based on a combination of clinical features, the ground-glass opacities in bilateral lungs.
results of chest CT and nucleic acid test. CT images showed multiple patchy ground-glass opaci-
ties in bilateral lungs (Fig.  7.1a–j), mainly located in sub-
pleural areas of the lung, accompanied with enlarged vessels
Q. Gan (*) · T. Hu · S. Jiang
Guangzhou Eighth People’s Hospital, Guangzhou Medical (Fig.  7.1f, h), thickened interlobular septa and intralobular
University, Guangzhou, China septa, and linear opacities (Fig. 7.1j).

© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 115
J. Liu et al. (eds.), Atlas of Chest Imaging in COVID-19 Patients, https://doi.org/10.1007/978-981-16-1082-0_7
116 Q. Gan et al.

a b

c d

Fig. 7.1  CT images showed multiple patchy ground-glass opacities in bilateral lungs (a–j), mainly located in subpleural areas of the lung, accom-
panied with enlarged vessels (f, h), thickened interlobular septa and intralobular septa, and linear opacities (a–j)
7  Role of CT and CT Features of Suspected COVID-19 Patients (PCR Negative) 117

g h

i j

Fig. 7.1 (continued)

7.3 Case 2 (Fig. 7.2a–j) 24, 2020 without obvious inducement. She was admitted
to the hospital on January 30, 2020. At the time of admis-
A 65-year-old female patient with a history of exposure to sion, the body temperature was 37.7 °C, the respiratory rate
the epidemic area presented with fever and chills on January was 18 breaths per minute, total white blood cell count was
118 Q. Gan et al.

a b

c d

e f

Fig. 7.2  CT images showed a segmental consolidation in the posterior segment of the upper lobe of the right lung with “air bronchogram” (c–g).
There was a small patchy increase in the density of the basal segment of the right lower lobe (h–j)

2.54 × 109 L, C-reactive protein was 20.09 mg/L, neutrophil 96.4%. The viral RNA in throat swab was negative in her
count was 1.25 × 109 L, lymphocyte count was 0.93 × 109 L, first examination. In her second examination, she was finally
platelet count was 147 × 109 L, and oxygen saturation was confirmed by Guangzhou CDC. On January 31, 2020, chest
7  Role of CT and CT Features of Suspected COVID-19 Patients (PCR Negative) 119

g h

i j

Fig. 7.2 (continued)

CT images revealed multiple patchy ground-glass opacities admitted to the hospital on January 30, 2020. At the time of
in bilateral lungs. admission, the body temperature was 36.6  °C, the respira-
CT images showed a segmental consolidation in the tory rate was 18 breaths per minute, total white blood cell
posterior segment of the upper lobe of the right lung with count was 5.08 × 109 L, C-reactive protein was 2.73 mg/L,
“air bronchogram” (Fig. 7.2c–g). There was a small patchy neutrophil count was 2.54  ×  109  L, lymphocyte count was
increase in the density of the basal segment of the right lower 2.09  ×  109  L, platelet count was 154  ×  109  L, and oxygen
lobe (Fig. 7.2h–j). saturation was 95.9%. The viral RNA in throat swab was
negative in her first examination. In her second examination,
she was finally confirmed by Guangzhou CDC. On January
7.4 Case 3 (Fig. 7.3a–j) 31, 2020, chest CT images showed multiple ground-glass
opacities in bilateral lungs.
A 63-year-old female patient had a history of exposure to CT images showed multiple ground-glass opaci-
epidemic areas. On January 28, 2020, she presented with ties (Fig.  7.3a–j) in the lower lobe of bilateral lungs
pharynx discomfort and expectoration, with no fever, no (Fig.  7.3d), with thickening of the interlobular septa
chest tightness or shortness of breath, no nausea or vomiting, (Fig.  7.3e–i) and linear opacities (Fig.  7.3j) in the left
and no abdominal distension or abdominal pain. She was lower lobe (Fig. 7.3j).
120 Q. Gan et al.

a b

c d

Fig. 7.3  CT images showed multiple ground-glass opacities (a–j) in the lower lobe of bilateral lungs (d), with thickening of the interlobular speta
(e–i) and linear opacities (j) in the left lower lobe (j)
7  Role of CT and CT Features of Suspected COVID-19 Patients (PCR Negative) 121

e f

g h

i j

Fig. 7.3 (continued)

7.5 Case 4 (Fig. 7.4a–j) fever and cough with no obvious inducement, and the clini-
cal symptoms improved after treatment. The next week, he
A 26-year-old male patient had a history of exposure to was readmitted with fever. At the time of admission, the
epidemic areas. On January 20, 2020, he presented with body temperature was 38.5  °C, the respiratory rate was
122 Q. Gan et al.

a b

c d

Fig. 7.4  CT images showed multiple nodular and patchy ground-glass opacities in both lungs, mainly located in the subpleural area of the lung
(a–j). The central structure of lobules was thickened (a white arrow, h black arrow)

18 breaths per minute, total white blood cell count was CT images showed multiple ground-glass opacities in bilat-
3.60 × 109 L, C-reactive protein was 5.3 mg/L, neutrophil eral lungs.
count was 1.26 × 109 L, lymphocyte count was 1.98 × 109 L, CT images showed multiple nodular and patchy ground-­
platelet count was 191 × 109 L, and oxygen saturation was glass opacities in both lungs, mainly located in the subpleu-
97.6%. The viral RNA in throat swab was negative in his ral area of the lung (Fig.  7.4a–j). The central structure of
first examination. In his second examination, he was finally lobules was thickened (Fig.  7.4a, white arrow; Fig.  7.4h,
confirmed by Guangzhou CDC. On January 31, 2020, chest black arrow).
7  Role of CT and CT Features of Suspected COVID-19 Patients (PCR Negative) 123

e f

g h

i j

Fig. 7.4 (continued)

7.6 Case 5 (Fig. 7.5a–j) C-reactive protein was 15.11  mg/L, neutrophil count was
3.88  ×  109  L, lymphocyte count was 2.42  ×  109  L, platelet
A 54-year-old female patient had a history of exposure to an count was 246 × 109 L, and oxygen saturation was 99%. The
epidemic area. On January 22, 2020, she presented with fever viral RNA in throat swab was negative in her first examina-
and fatigue, accompanied by headache, muscle ache, cough, tion. In her second examination, she was finally confirmed
sputum, and slight shortness of breath after exercise. Chest by Guangzhou CDC. On January 25, 2020, chest CT images
x-ray showed pneumonia, and she was admitted to the hospi- showed multiple ground-glass opacities in bilateral lungs.
tal on January 24, 2020. At the time of admission, the body CT images showed multiple patchy ground-glass opaci-
temperature was 36.1 °C, the respiratory rate was 21 breaths ties in bilateral lungs with enlarged vessels in the lesions
per minute, total white blood cell count was 6.77  ×  109  L, (Fig. 7.5j).
124 Q. Gan et al.

a b

c d

Fig. 7.5  CT images showed multiple patchy ground-glass opacities in bilateral lungs with enlarged vessels in the lesions (j)
7  Role of CT and CT Features of Suspected COVID-19 Patients (PCR Negative) 125

e f

g h

i j

Fig. 7.5 (continued)

7.7 Case 6 (Fig. 7.6a–j) count was 0.95 × 109 L, platelet count was 101 × 109 L, and
oxygen saturation was 99.6%. The viral RNA in throat swab
A 57-year-old male patient with a history of exposure to epi- was negative in his first examination. In his second exami-
demic areas presented with chills and fever on January 26, nation, he was finally confirmed by Guangzhou CDC.  On
2020. He was admitted to the hospital on February 1, 2020. February 5, 2020, chest CT images showed multiple ground-­
At the time of admission, the body temperature was 37 °C, glass opacities in bilateral lungs.
the respiratory rate was 20 breaths per minute, total white CT images showed multiple patchy ground-glass opaci-
blood cell count was 6.77  ×  109  L, C-reactive protein was ties in bilateral lungs with enlarged vessels in the lesions
18.50 mg/L, neutrophil count was 5.28 × 109 L, lymphocyte (Fig. 7.6j).
126 Q. Gan et al.

a b

c d

Fig. 7.6  CT images showed multiple patchy ground-glass opacities in bilateral lungs with enlarged vessels in the lesions (j)
7  Role of CT and CT Features of Suspected COVID-19 Patients (PCR Negative) 127

e f

g h

i j

Fig. 7.6 (continued)

was admitted to the hospital on January 28, 2020. At the


7.8 Case 7 (Fig. 7.7a–j) time of admission, the body temperature was 37.8  °C,
the respiratory rate was 18 breaths per minute, total
A 70-year-old male patient with a history of exposure white blood cell count was 7.05 × 10 9 L, C-reactive pro-
to epidemic areas presented with cough and fever. He tein was 92.82 mg/L, neutrophil count was 6.21 × 10 9 L,
128 Q. Gan et al.

a b

c d

e f

Fig. 7.7  CT images showed multiple patchy ground-glass opacities and linear opacities with interlobular septal thickening in bilateral lungs (j)

lymphocyte count was 0.56  ×  109  L, platelet count was CT images showed multiple ground-glass opacities in
175 × 10 9 L, and oxygen saturation was 92.5%. The viral bilateral lungs.
RNA in throat swab was negative in his first examina- CT images showed multiple patchy ground-glass opaci-
tion. In his second examination, he was finally con- ties and linear opacities with interlobular septal thickening
firmed by Guangzhou CDC. On January 30, 2020, chest in bilateral lungs (Fig. 7.7j).
7  Role of CT and CT Features of Suspected COVID-19 Patients (PCR Negative) 129

g h

i j

Fig. 7.7 (continued)

7.9 Case 8 (Fig. 7.8a–j) 1.97  ×  109  L, lymphocyte count was 1.11  ×  109  L, plate-
let count was 149 × 109 L, and oxygen saturation was 99%.
A 62-year-old female patient with a history of exposure The viral RNA in throat swab was negative for two examina-
to epidemic areas presented with cough and fever without tions. In her third examination, she was finally confirmed by
obvious inducement on February 1, 2020. She was admit- Guangzhou CDC.  On February 5, 2020, chest CT images
ted to the hospital on February 3, 2020. At admission, the showed multiple ground-glass opacities in bilateral lungs.
body temperature was 39  °C, the respiratory rate was 20 CT images showed multiple patchy ground-glass opaci-
breaths per minute, white blood cell count was 3.75 × 109 L, ties with blurred margin and thickened interlobular septa in
C-reactive protein was 18.67  mg/L, neutrophil count was bilateral lungs (Fig. 7.8a–j).
130 Q. Gan et al.

a b

c d

e f

Fig. 7.8  CT images showed multiple patchy ground-glass opacities with blurred margin and thickened interlobular septa in bilateral lungs (a–j)
7  Role of CT and CT Features of Suspected COVID-19 Patients (PCR Negative) 131

g h

i j

Fig. 7.8 (continued)

7.10 Case 9 (Fig. 7.9a–j) count was 239 × 109 L, and oxygen saturation was 82.9%.
The viral RNA in throat swab was negative for two examina-
A 43-year-old male patient with a history of exposure to epi- tions. In his third examination, he was finally confirmed by
demic areas presented with cough and fever without obvi- Guangzhou CDC.  On February 5, 2020, chest CT images
ous inducement on January 22, 2020. He was admitted to showed multiple ground-glass opacities and patchy consoli-
the hospital on February 5, 2020. Admission temperature dation in bilateral lungs.
was 37.7  °C, the respiratory rate was 20 breaths per min- CT images showed multiple patchy ground-glass opaci-
ute, peripheral white blood cell count was 4.2  ×  109  L, ties, consolidation, and thickening of the interlobular septa
C-reactive protein was 78.56  mg/L, neutrophil count was (Fig.  7.9a–j) in bilateral lungs. “Air bronchogram” can be
2.50 × 109 L, lymphocyte count was 1.23 × 109 L, platelet seen in the upper lobe of the left lung (Fig. 7.9j).
132 Q. Gan et al.

a b

c d

e f

Fig. 7.9  CT images showed multiple patchy ground-glass opacities, consolidation, and thickening of the interlobular septa (a–j) in bilateral lungs.
“Air bronchogram” can be seen in the upper lobe of the left lung (j)
7  Role of CT and CT Features of Suspected COVID-19 Patients (PCR Negative) 133

g h

i j

Fig. 7.9 (continued)

7.11 Case 10 (Fig. 7.10a–j) viral RNA in throat swab was negative for four examina-
tions. In his fifth examination, he was finally confirmed by
A 23-year-old male patient with a history of close contact Guangzhou CDC.  On January 29, 2020, chest CT images
with a confirmed patient was admitted to the hospital on showed multiple ground-glass opacities and multiple patchy
January 23, 2020. At the time of admission, the body tem- consolidation in the right lower lobe.
perature was 36.3  °C, the respiratory rate was 18 breaths CT images showed multiple patchy ground-glass
per minute, total white blood cell count was 4.23 × 109 L, opacities and focal consolidation in the lower lobe of the
C-reactive protein was 18.4  mg/L, neutrophil count was right lung (Fig. 7.10b, white arrow); “paving stone sign”
2.23 × 109 L, lymphocyte count was 1.53 × 109 L, platelet (Fig.  7.10h) and “air bronchogram sign” (Fig.  7.10j) can
count was 187 × 109 L, and oxygen saturation was 98%. The be seen.
134 Q. Gan et al.

a b

c d

e f

Fig. 7.10  CT images showed multiple patchy ground-glass opacities and focal consolidation in the lower lobe of the right lung (b white arrow);
“paving stone sign” (h) and “air bronchogram sign” (j) can be seen
7  Role of CT and CT Features of Suspected COVID-19 Patients (PCR Negative) 135

g h

i j

Fig. 7.10 (continued)

6. Ju LE, Ri O, Christian L, et  al. Pattern of early human-to-­


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(Epub ahead of print).
Follow-Up CT of Patients with First
Negative CT But Positive PCR 8
for COVID-19

Zhoukun Ling, Deyang Huang, and Chunliang Lei

8.1 Introduction Because of the complex clinical situation among


COVID-­19 patients, chest CT examinations should be per-
A recent outbreak of coronavirus disease 2019 (COVID-19) formed multiple times if possible and necessary for diagno-
has become a public health emergency of international con- sis and monitoring purposes.
cern [1]. As of April 7, 2020, the coronavirus named as severe
acute respiratory syndrome coronavirus 2 SARS-­CoV-­2 has
infected more than 1,210,956 individuals, and caused 67,594 8.2 Case 1 (Fig. 8.1a–l)
fatal cases [2].
In a familial cluster of COVID-19 pneumonia [3], a A 66-year-old male was admitted without any symptoms. He
10-year-old child had no clinical symptoms, but showed had exposed in the epidemic area. Fever and chest tightness
ground-glass lung opacification on CT, was viral RNA posi- occurred on day-1 of admission, and the highest tempera-
tive in subsequent laboratory test. This study supports that ture in the course of the disease was 38.6 °C. White blood
lung damage by viral infection is not necessary to result in cell count, lymphocyte count, and C-reactive protein were
obvious the clinical symptoms. 5.41  ×  109/L, 0.98  ×  109/L, and <10  mg/L, respectively.
We observed 295 patients with laboratory-identified The patient was laboratory confirmed by novel coronavirus
SARS-CoV-2 infection by RT-PCR between January 23, nucleic acid throat swab test in Guangzhou CDC. Chest CT
2020 and February 18, 2020 in Guangzhou Eighth People’s examination was performed on 1 day (Fig. 8.1a, b), 5 days
Hospital. Among them, 49 (17%) patients presented nega- (Fig. 8.1c, d), 8 days (Fig. 8.1e, f), and 10 days (Fig. 8.1g–l)
tive chest CT images at initial presentation; however, they after onset of symptoms, respectively.
had positive findings in the following CT scans after 3–14 On 1 day after onset of symptoms, chest CT images
days of onset. Most patients had no clinical symptoms or showed no obvious abnormalities in both lungs (Fig. 8.1a, b);
mild symptoms. According to the report of Lirong Zou On 5 days after onset of symptoms, chest CT images showed
et  al., the asymptomatic and symptomatic patients showed multiple patchy ground-glass opacities in both lungs, pre-
similar viral loads [4]. Above findings suggest that suspected senting “crazy paving sign” (Fig. 8.1c, d); On 8 days after
patients are also the potential sources of infection, thus indi- onset of symptoms, chest CT images demonstrated enlarged
vidual isolation plays an important role in curbing the spread lesions and increased density of the lesions, compared with
of COVID-19. previous images, indicating disease progression, and the
For those viral infected patients with the initial negative “crazy paving sign” was seen (Fig. 8.1e, f white arrow); On
chest CT scan, some patients advance to the stage with nota- 10 days after onset of symptoms, chest CT images demon-
ble new lung lesions during the following chest CT reexami- strated enlarged lesions and increased density of the lesions,
nation, while some patients keep persistently negative CT compared with previous images, and both lungs showed
images until they met discharge criteria. “white lung” changes (Fig. 8.1g, h); the coronal and sagit-
tal positions show diffuse distribution of the lung lesions
(Fig.  8.1i–l), showing thickening of the interlobar pleura
(Fig. 8.1l white arrow).
Z. Ling (*) · D. Huang · C. Lei
Guangzhou Eighth People’s Hospital, Guangzhou Medical
University, Guangzhou, China

© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 137
J. Liu et al. (eds.), Atlas of Chest Imaging in COVID-19 Patients, https://doi.org/10.1007/978-981-16-1082-0_8
138 Z. Ling et al.

a b

c d

e f

Fig. 8.1  On 1 day after onset of symptoms, chest CT images showed seen (e, f white arrow); On 10 days after onset of symptoms, chest CT
no obvious abnormalities in both lungs (a, b); On 5 days after onset of images demonstrated enlarged lesions and increased density of the
symptoms, chest CT images showed multiple patchy ground-glass lesions, compared with previous images, and both lungs showed “white
opacities in both lungs, presenting “crazy paving sign” (c, d); On 8 days lung” changes (g, h); the coronal and sagittal positions show diffuse
after onset of symptoms, chest CT images demonstrated enlarged distribution of the lung lesions (i–l), showing thickening of the interlo-
lesions and increased density of the lesions, compared with previous bar pleura (l white arrow)
images, indicating disease progression, and the “crazy paving sign” was
8  Follow-Up CT of Patients with First Negative CT But Positive PCR for COVID-19 139

g h

i j

k l

Fig. 8.1 (continued)
140 Z. Ling et al.

8.3 Case 2 (Fig. 8.2a–l) were 5.17 × 109/L, 1.31 × 109/L, and <10 mg/L, respectively.


The patient was laboratory confirmed by novel coronavi-
A 41-year-old male was admitted with fever for 3 days, accom- rus nucleic acid throat swab test in Guangzhou CDC. Chest
panied by chills and cough. He had exposed in the epidemic CT examination was performed on 4 days (Fig. 8.2a, b), 10
area. The body temperature at admission was 37.5 °C. White days (Fig. 8.2c, d), 14 days (Fig. 8.2e, f, i, k), and 18 days
blood cell count, lymphocyte count, and C-reactive protein (Fig. 8.2g, h, j, l) after onset of symptoms, respectively.

a b

c d

e f

Fig. 8.2  On the 4th day after onset, the first chest CT on 4 days after after onset of symptoms, chest CT images demonstrated enlarged
onset of symptoms, chest CT images showed no obvious abnormality in lesions and increased density of the lesions, compared with previous
both lungs (a, b). On 10 days after onset of symptoms, chest CT images images, indicating disease progression, and the “crazy paving sign” and
showed patchy ground-glass opacities in the upper lobe of the right lung subpleural curvilinear line were seen (g white arrow and h). The coro-
(c), and no obvious abnormality was observed in the lower lobe of both nal and sagittal images showed patchy ground-glass opacities of both
lungs (d). On 14 days after onset of symptoms, chest CT images showed lungs (i–l)
multiple patchy ground-glass opacities in both lungs (e, f). On 18 days
8  Follow-Up CT of Patients with First Negative CT But Positive PCR for COVID-19 141

g h

i j

k l

Fig. 8.2 (continued)
142 Z. Ling et al.

On the 4th day after onset, the first chest CT on 4 days 37.4  °C.  White blood cell count, lymphocyte count, and
after onset of symptoms, chest CT images showed no obvi- C-reactive protein were 11.02  ×  109/L, 3.02  ×  109/L, and
ous abnormality in both lungs (Fig.  8.2a, b). On 10 days <10  mg/L, respectively. The patient was laboratory con-
after onset of symptoms, chest CT images showed patchy firmed by novel coronavirus nucleic acid throat swab test
ground-­glass opacities in the upper lobe of the right lung in Guangzhou CDC. Chest CT examination was performed
(Fig. 8.2c), and no obvious abnormality was observed in the on 5 days (Fig.  8.3a, b), 10 days (Fig.  8.3c, d), 14 days
lower lobe of both lungs (Fig. 8.2d). On 14 days after onset (Fig. 8.3e, f), and 17 days (Fig. 8.3g–l) after onset of symp-
of ­symptoms, chest CT images showed multiple patchy toms, respectively.
ground-glass opacities in both lungs (Fig.  8.2e, f). On 18 On 5 days after onset of symptoms, chest CT images
days after onset of symptoms, chest CT images demonstrated showed no obvious abnormality in both lungs (Fig.  8.3a,
enlarged lesions and increased density of the lesions, com- b). On 10 days after onset of symptoms, chest CT images
pared with previous images, indicating disease progression, showed patchy ground-glass opacities in both lungs
and the “crazy paving sign” and subpleural curvilinear line (Fig. 8.3c, d). On 14 days after onset of symptoms, chest
were seen (Fig. 8.2g white arrow and Fig. 8.2h). The coronal CT images demonstrated enlarged lesions and increased
and sagittal images showed patchy ground-glass opacities of density of the lesions, compared with previous images, indi-
both lungs (Fig. 8.2i–l). cating disease progression (Fig. 8.3e, f). On 17 days after
onset of symptoms, chest CT images showed decreased
lesions in bilateral lungs, and subpleural arc band shadow
8.4 Case 3 (Fig. 8.3a–l) in the lower lobe of both lungs. The lesions gradually
disappeared/vanished (Fig.  8.3g, h). Coronal and sagit-
A 44-year-old male was admitted with fever for 3 days, tal images showed patchy ground-glass opacities in both
accompanied by chills and cough. He had exposed in the lungs (Fig. 8.3i–l), and “reverse halo sign” was seen locally
epidemic area. The body temperature at admission was (Fig. 8.3j, l white arrow).
8  Follow-Up CT of Patients with First Negative CT But Positive PCR for COVID-19 143

a b

c d

e f

Fig. 8.3  On 5 days after onset of symptoms, chest CT images showed On 17 days after onset of symptoms, chest CT images showed decreased
no obvious abnormality in both lungs (a, b). On 10 days after onset of lesions in bilateral lungs, and subpleural arc band shadow in the lower
symptoms, chest CT images showed patchy ground-glass opacities in lobe of both lungs. The lesions gradually disappeared/vanished (g, h).
both lungs (c, d). On 14 days after onset of symptoms, chest CT images Coronal and sagittal images showed patchy ground-glass opacities in
demonstrated enlarged lesions and increased density of the lesions, both lungs (i–l), and “reverse halo sign” was seen locally (j, l white
compared with previous images, indicating disease progression (e, f). arrow)
144 Z. Ling et al.

g h

i j

k l

Fig. 8.3 (continued)
8  Follow-Up CT of Patients with First Negative CT But Positive PCR for COVID-19 145

8.5 Case 4 (Fig. 8.4a–l) and C-reactive protein were 3.74 × 109/L, 1.49 × 109/L, and
<10  mg/L, respectively. The patient was laboratory con-
A 41-year-old male was admitted with fever for 3 days, firmed by novel coronavirus nucleic acid throat swab test
accompanied by pharyngeal dryness and cough. He had in Guangzhou CDC. Chest CT examination was performed
exposed in the epidemic area. The body temperature at admis- on 4 days (Fig. 8.4a, b), 8 days (Fig. 8.4c, d, i, j), 11 days
sion was 37.3 °C. White blood cell count, lymphocyte count, (Fig. 8.4e, f, k), and 16 days (Fig. 8.4g, h, l), respectively.

a b

c d

e f

Fig. 8.4  On 4 days after onset of symptoms, chest CT images showed ease progression (e, f). On 16 days after onset of symptoms, chest CT
no obvious abnormality in both lungs (a, b). On 8 days after onset of images showed that the scope of the lesion in the lower lobe of the right
symptoms, chest CT images showed patchy ground-glass opacities in lung was smaller than before (g, h). Coronal and sagittal images showed
the lower lobe of the right lung (c, d). On 11 days after onset of symp- patchy ground-glass opacities in the lower lobe of the right lung (i–l),
toms, chest CT images demonstrated enlarged lesions and increased and “reverse halo sign” in the dorsal segment of the lower lobe of the
density of the lesions, compared with previous images, indicating dis- right lung (k white arrow)
146 Z. Ling et al.

g h

i j

k l

Fig. 8.4 (continued)
8  Follow-Up CT of Patients with First Negative CT But Positive PCR for COVID-19 147

On 4 days after onset of symptoms, chest CT images Guangzhou CDC. Chest CT examination was performed on
showed no obvious abnormality in both lungs (Fig.  8.4a, 3 days (Fig. 8.5a), 6 days (Fig. 8.5b), 10 days (Fig. 8.5c, g,
b). On 8 days after onset of symptoms, chest CT images i), 13 days (Fig. 8.5d, h), 16 days (Fig. 8.5e), and 24 days
showed patchy ground-glass opacities in the lower lobe of (Fig. 8.5f, j) after onset of symptoms, respectively.
the right lung (Fig. 8.4c, d). On 11 days after onset of symp- On 3 days after onset of symptoms, chest CT images
toms, chest CT images demonstrated enlarged lesions and showed no obvious abnormalities in both lungs (Fig. 8.5a).
increased density of the lesions, compared with previous On 6 days after onset of symptoms, chest CT images showed
images, indicating disease progression (Fig. 8.4e, f). On 16 patchy ground-glass opacities in the lower lobe of the left
days after onset of symptoms, chest CT images showed that lung (Fig. 8.5b). On 10 days after onset of symptoms, chest
the scope of the lesion in the lower lobe of the right lung CT images showed new lesions in the right lung, increased
was smaller than before (Fig. 8.4g, h). Coronal and sagittal density of lesions in the lower lobe of the left lung, and
images showed patchy ground-glass opacities in the lower pleural subline (Fig. 8.5c). On 13 days after onset of symp-
lobe of the right lung (Fig. 8.4i–l), and “reverse halo sign” toms, chest CT images showed that the lesion in the lower
in the dorsal segment of the lower lobe of the right lung lobe of both lungs was slightly more absorbed than before,
(Fig. 8.4k white arrow). with strip-shaped shadows (Fig.  8.5d). On 16 days after
onset of symptoms, chest CT images showed no significant
changes in the bilateral lung lesions (Fig. 8.5e). On 24 days
8.6 Case 5 (Fig. 8.5a–j) after onset of symptoms, chest CT images showed that the
lesions in bilateral lungs were more absorbed than before,
A 50-year-old male was admitted with pharyngeal discom- with strip-­shaped shadows (Fig. 8.5f). Coronal and sagittal
fort for 1 day. He had exposed to confirmed cases with novel images showed multiple patchy ground-glass opacities and
coronavirus pneumonia. The body temperature at admission strip-­shaped shadows in both lungs (Fig. 8.5g, h). Multiple
was 36.3  °C.  White blood cell count, lymphocyte count, strip-­shaped shadows were seen under the pleura in the lower
and C-reactive protein were 5.85 × 109/L, 0.86 × 109/L, and lobe of the right lung (Fig. 8.5i). The range of lesions in the
<10  mg/L, respectively. The patient was laboratory con- right lung was smaller than before, and the pleural subline
firmed by novel coronavirus nucleic acid throat swab test in was seen (Fig. 8.5j white arrow).
148 Z. Ling et al.

a b

c d

e f

Fig. 8.5  On 3 days after onset of symptoms, chest CT images showed toms, chest CT images showed no significant changes in the bilateral
no obvious abnormalities in both lungs (a). On 6 days after onset of lung lesions (e). On 24 days after onset of symptoms, chest CT images
symptoms, chest CT images showed patchy ground-glass opacities in showed that the lesions in bilateral lungs were more absorbed than
the lower lobe of the left lung (b). On 10 days after onset of symptoms, before, with strip-shaped shadows (f). Coronal and sagittal images
chest CT images showed new lesions in the right lung, increased den- showed multiple patchy ground-glass opacities and strip-shaped shad-
sity of lesions in the lower lobe of the left lung, and pleural subline (c). ows in both lungs (g, h). Multiple strip-shaped shadows were seen
On 13 days after onset of symptoms, chest CT images showed that the under the pleura in the lower lobe of the right lung (i). The range of
lesion in the lower lobe of both lungs was slightly more absorbed than lesions in the right lung was smaller than before, and the pleural subline
before, with strip-shaped shadows (d). On 16 days after onset of symp- was seen (j white arrow)
8  Follow-Up CT of Patients with First Negative CT But Positive PCR for COVID-19 149

g h

i j

Fig. 8.5 (continued)

8.7 Case 6 (Fig. 8.6a–l) were 5.65 × 109/L, 2.79 × 109/L, and <10 mg/L, respec-


tively. The patient was laboratory confirmed by novel
A 47-year-old male was admitted with fever for 4 days, coronavirus nucleic acid throat swab test in Guangzhou
accompanied by pharyngalgia and cough. He had exposed CDC.  Chest CT examination was performed on 7 days
to confirmed cases with novel coronavirus pneumonia. (Fig. 8.6a, b), 11 days (Fig. 8.6c, d), days 16 (Fig. 8.6e, f,
The body temperature at admission was 37.6  °C.  White i, k), and days 21 (Fig. 8.6g, h, j, l) after onset of symp-
blood cell count, lymphocyte count, and C-reactive protein toms, respectively.
150 Z. Ling et al.

a b

c d

e f

Fig. 8.6  On 7 days after onset of symptoms, chest CT images showed no before (e, f). On 21 days after onset of symptoms, chest CT images dem-
obvious abnormality in both lungs (a, b). On 11 days after onset of symp- onstrated enlarged lesions and increased density of the lesions, compared
toms, chest CT images showed nodular/patchy ground-glass opacities in with previous images, indicating disease progression (g, h). Coronal and
the upper and lower lobes of the left lung (c, d), and thickened vascular sagittal images showed patchy ground-glass opacities in the upper lobe of
shadows in the lesions in the upper lobe of the left lung (c, e). On 16 days the left lung (i–l), and “crazy paving sign” in the posterior segment of the
after onset of symptoms, chest CT images showed more lesions than upper lobe tip of the left lung (l empty arrow)

On 7 days after onset of symptoms, chest CT images lung (Fig.  8.6c, e). On 16 days after onset of symptoms,
showed no obvious abnormality in both lungs (Fig.  8.6a, chest CT images showed more lesions than before (Fig. 8.6e,
b). On 11 days after onset of symptoms, chest CT images f). On 21 days after onset of symptoms, chest CT images
showed nodular/patchy ground-glass opacities in the upper demonstrated enlarged lesions and increased density of the
and lower lobes of the left lung (Fig. 8.6c, d), and thickened lesions, compared with previous images, indicating dis-
vascular shadows in the lesions in the upper lobe of the left ease progression (Fig. 8.6g, h). Coronal and sagittal images
8  Follow-Up CT of Patients with First Negative CT But Positive PCR for COVID-19 151

g h

i j

k l

Fig. 8.6 (continued)
152 Z. Ling et al.

showed patchy ground-glass opacities in the upper lobe of days (Fig. 8.7c, d, i), 12 days (Fig. 8.7e, f, k), and 22 days
the left lung (Fig. 8.6i–l), and “crazy paving sign” in the pos- (Fig. 8.7g, h, j, l) after onset of symptoms, respectively.
terior segment of the upper lobe tip of the left lung (Fig. 8.6l On 5 days after onset of symptoms, chest CT images
empty arrow). showed no obvious abnormalities in both lungs (Fig.  8.7a,
b). On 9 days after onset of symptoms, chest CT images
showed patchy ground-glass opacities in the lower lobe
8.8 Case 7 (Fig. 8.7a–l) of the right lung (Fig.  8.7c, d). On 12 days after onset of
symptoms, chest CT images showed that the density of
A 45-year-old male was admitted with fever for 4 days, lesions in the lower lobe of the right lung was higher than
accompanied by cough and sputum for 3 days. He had before (Fig.  8.7e, f). On 22 days after onset of symptoms,
exposed to confirmed cases with novel coronavirus pneumo- chest CT images showed that the scope and density of the
nia. The body temperature at admission was 37.3 °C. White lesion in the lower lobe of the right lung were smaller than
blood cell count, lymphocyte count, and C-reactive protein before (Fig. 8.7g, h), and the lesion in the lower lobe of the
were 4.59 × 109/L, 2.10 × 109/L, and <10 mg/L, respectively. right lung presented strip-shaped shadows after absorption
The patient was laboratory confirmed by novel coronavi- (Fig. 8.7g empty arrow). Patchy ground-glass opacities were
rus nucleic acid throat swab test in Guangzhou CDC. Chest seen in the lower lobe of the right lung at coronal and sagittal
CT examination was performed on 5 days (Fig. 8.7a, b), 9 positions (Fig. 8.7i–k).
8  Follow-Up CT of Patients with First Negative CT But Positive PCR for COVID-19 153

a b

c d

e f

Fig. 8.7  On 5 days after onset of symptoms, chest CT images showed onset of symptoms, chest CT images showed that the scope and density
no obvious abnormalities in both lungs (a, b). On 9 days after onset of of the lesion in the lower lobe of the right lung were smaller than before
symptoms, chest CT images showed patchy ground-glass opacities in (g, h), and the lesion in the lower lobe of the right lung presented strip-­
the lower lobe of the right lung (c, d). On 12 days after onset of symp- shaped shadows after absorption (g empty arrow). Patchy ground-glass
toms, chest CT images showed that the density of lesions in the lower opacities were seen in the lower lobe of the right lung at coronal and
lobe of the right lung was higher than before (e, f). On 22 days after sagittal positions (i–k)
154 Z. Ling et al.

g h

i j

k l

Fig. 8.7 (continued)
8  Follow-Up CT of Patients with First Negative CT But Positive PCR for COVID-19 155

8.9 Case 8 (Fig. 8.8a–j) 2.05  ×  109/L, and <10  mg/L, respectively. The patient was
laboratory confirmed by novel coronavirus nucleic acid throat
A 45-year-old male patient was admitted with fever and cough swab test in Guangzhou CDC. Chest CT examination was per-
for 2 days. He had exposed in the epidemic area. The body formed on 3 days (Fig.  8.8a), 7 days (Fig.  8.8b, i), 10 days
temperature at admission was 38.0 °C. White blood cell count, (Fig. 8.8c, g), 15 days (Fig. 8.8d) 19 days (Fig. 8.8e), and 21
lymphocyte count, and C-reactive protein were 5.35 × 109/L, days (Fig. 8.8f, h, j) after onset of symptoms, respectively.

a b

c d

e f

Fig. 8.8  On 3 days after onset of symptoms, chest CT images showed toms, chest CT images showed that the scope of the lesion in the lower
stripy shadows in the middle lobe of the right lung (a). On 7 days after lobe of the right lung was smaller than before, with strip-shaped shad-
onset of symptoms, chest CT images showed patchy ground-glass ows (d, e). On 21 days after onset of symptoms, chest CT images
opacities in the lower lobe of the right lung (b). On 10 days after onset showed that the lesion in the lower lobe of the right lung disappeared
of symptoms, chest CT images showed an enlarged lesion in the lower (f). Scattered patchy ground-glass opacities were seen in the upper lobe
lobe of the right lung (c). On 15 days and 19 days after onset of symp- of the right lung at coronal and sagittal positions (g–j)
156 Z. Ling et al.

g h

i j

Fig. 8.8 (continued)

On 3 days after onset of symptoms, chest CT images showed toms, chest CT images showed that the scope of the lesion in
stripy shadows in the middle lobe of the right lung (Fig. 8.8a). the lower lobe of the right lung was smaller than before, with
On 7 days after onset of symptoms, chest CT images showed strip-shaped shadows (Fig. 8.8d, e). On 21 days after onset of
patchy ground-glass opacities in the lower lobe of the right symptoms, chest CT images showed that the lesion in the lower
lung (Fig. 8.8b). On 10 days after onset of symptoms, chest CT lobe of the right lung disappeared (Fig. 8.8f). Scattered patchy
images showed an enlarged lesion in the lower lobe of the right ground-glass opacities were seen in the upper lobe of the right
lung (Fig. 8.8c). On 15 days and 19 days after onset of symp- lung at coronal and sagittal positions (Fig. 8.8g–j).
8  Follow-Up CT of Patients with First Negative CT But Positive PCR for COVID-19 157

8.10 Case 9 (Fig. 8.9a–j) firmed by novel coronavirus nucleic acid throat swab test in
Guangzhou CDC. Chest CT examination was performed on
A 43-year-old female was admitted with pharyngalgia for 1 1 day (Fig. 8.9a), 5 days (Fig. 8.9b), 8 days (Fig. 8.9c), 11
day. She had exposed to confirmed cases with novel corona- days (Fig. 8.9d, g, i), 14 days (Fig. 8.9e, h, j), and 18 days
virus pneumonia. White blood cell count, lymphocyte count, (Fig. 8.9f) after onset of symptoms, respectively.
and C-reactive protein were 4.44 × 109/L, 0.86 × 109/L, and On 1 day after onset of symptoms, chest CT images showed
<10  mg/L, respectively. The patient was laboratory con- no obvious abnormalities in both lungs (Fig. 8.9a). On 5 days

a b

c d

e f

Fig. 8.9  On 1 day after onset of symptoms, chest CT images showed lobe of the right lung (c, d). On 14 and 18 days after onset of symptoms,
no obvious abnormalities in both lungs (a). On 5 days after onset of chest CT images showed that the lesion was smaller, and the density is
symptoms, chest CT images showed patchy ground-glass opacities in lower than before (e, f). Patchy ground-glass opacities were seen in the
the lower lobe of the right lung (b). On 8 days and 11 days after onset lower lobe of the right lung at coronal and sagittal positions (g–j)
of symptoms, chest CT images showed increased lesions in the lower
158 Z. Ling et al.

g h

i j

Fig. 8.9 (continued)

after onset of symptoms, chest CT images showed patchy 8.11 Case 10 (Fig. 8.10a–j)
ground-glass opacities in the lower lobe of the right lung
(Fig. 8.9b). On 8 days and 11 days after onset of symptoms, A 45-year-old female was admitted with fever for 2 days,
chest CT images showed increased lesions in the lower lobe of accompanied by cough. She had exposed to confirmed cases
the right lung (Fig. 8.9c, d). On 14 and 18 days after onset of with novel coronavirus pneumonia. The body temperature
symptoms, chest CT images showed that the lesion was smaller, at admission was 37.5  °C.  White blood cell count, lym-
and the density is lower than before (Fig. 8.9e, f). Patchy ground- phocyte count, and C-reactive protein were 7.11  ×  109/L,
glass opacities were seen in the lower lobe of the right lung at 0.61 × 109/L, and <10 mg/L, respectively. The patient was
coronal and sagittal positions (Fig. 8.9g–j). laboratory confirmed by novel coronavirus nucleic acid
8  Follow-Up CT of Patients with First Negative CT But Positive PCR for COVID-19 159

a b

c d

e f

Fig. 8.10  On 3 days after onset of symptoms, chest CT images showed of the lesion in the lower lobe of the right lung (e). On 23 days after
no obvious abnormalities in both lungs (a). On 6 days after onset of onset of symptoms, chest CT images showed the lesion in the lower
symptoms, chest CT images showed new nodular ground-glass opaci- lobe of the right lung disappeared (f). At the coronal and sagittal posi-
ties in the lower lobe of the right lung, and the thickening of the central tion, a small nodular ground hyaline density shadow was seen in the
structure of the lobule was observed (b). On 10 days and 13 days after lower lobe of the right lung, and the central node of the lobule was
onset of symptoms, chest CT images showed a slightly larger range of thickened (g, i empty arrow), and the lesion disappeared after treatment
lesions in the lower lobe of the right lung (c, d). On 18 days after onset (h, j white arrow)
of symptoms, chest CT images showed a slight decrease in the density
160 Z. Ling et al.

g h

i j

Fig. 8.10 (continued)

throat swab test in Guangzhou CDC. Chest CT examination On 3 days after onset of symptoms, chest CT
was performed on 3 days (Fig.  8.10a), 6 days (Fig.  8.10b, images showed no obvious abnormalities in both lungs
g, i), 10 days (Fig.  8.10c), 13 days (Fig.  8.10d), 18 days (Fig.  8.10a). On 6 days after onset of symptoms, chest
(Fig.  8.10e), and 23 days (Fig.  8.10f, h, j) after onset of CT images showed new nodular ground-glass opacities in
symptoms, respectively. the lower lobe of the right lung, and the thickening of the
8  Follow-Up CT of Patients with First Negative CT But Positive PCR for COVID-19 161

central structure of the lobule was observed (Fig. 8.10b). References


On 10 days and 13 days after onset of symptoms, chest
CT images showed a slightly larger range of lesions in 1. Zhu N, Zhang D, Wang W, et al. A novel coronavirus from patients
the lower lobe of the right lung (Fig.  8.10c, d). On 18 with pneumonia in China, 2019. N Engl J Med. 2020;382(8):727–
33. https://doi.org/10.1056/NEJMoa2001017.
days after onset of symptoms, chest CT images showed 2. World Health Organization (WHO). Coronavirus disease 2019

a slight decrease in the density of the lesion in the lower (COVID-19) situation report-78. https://www.who.int/docs/
lobe of the right lung (Fig. 8.10e). On 23 days after onset default-­source/coronaviruse/situation-­reports/20200407-­sitrep-­78-­
of symptoms, chest CT images showed the lesion in the covid-­19.pdf?sfvrsn=bc43e1b_2
3. Chan JF, Yuan S, Kok KH, et  al. A familial cluster of pneu-

lower lobe of the right lung disappeared (Fig. 8.10f). At monia associated with the 2019 novel coronavirus indi-
the coronal and sagittal position, a small nodular ground cating person-to-person transmission: a study of a family
hyaline density shadow was seen in the lower lobe of the cluster. Lancet. 2020;395(10223):514–23. https://doi.org/10.1016/
right lung, and the central node of the lobule was thick- S0140-­6736(20)30154-­9.
4. Zou L, Ruan F, Huang M, et  al. SARS-CoV-2 viral load in

ened (Fig.  8.10g, i empty arrow), and the lesion disap- upper respiratory specimens of infected patients. N Engl J Med.
peared after treatment (Fig. 8.10h, j white arrow). 2020;382(12):1177–9. https://doi.org/10.1056/NEJMc2001737.
Imaging Analysis of Family Clustering
COVID-19 9
Rui Jiang, Xiaoneng Mo, and Yueping Li

9.1 Introduction As of February 11, 20 provinces outside of Hubei had


reported 1183 clusters of cases, 88% of which contained 2–4
According to the four items in the sixth edition of the “New confirmed cases [2]. More notably, 64% of the clusters
Coronavirus Infection Pneumonia Diagnosis and Treatment recorded to date were within families. Family clustering [3]
Program” diagnostic criteria, if any two of the clinical mani- is characterized by rapid nucleic acid testing when members
festations are met, suspected infection can be diagnosed. of the family have a history of contact with infected areas
and early onset of fever-related symptoms, which facilitates
1. A history of travel or residence in disease-relative area [1] timely identification of COVID-19 patients [4]. During the
and its surrounding areas, or other communities with epidemic, Guangzhou CDC worked quickly to grasp the
reported cases, within 14 days before the onset of onset of symptoms in family members of infected patients,
illness; so some patients were isolated and treated early before
2. Have a history of contact with a new coronavirus infec- symptoms appeared.
tion (positive nucleic acid test) within 14 days before
onset;
3. Have contacted patients with fever or respiratory symp- 9.2 Family 1
toms from Wuhan and its surrounding areas, or from
communities with case reports within 14 days before Families in this group: the mother first developed symptoms
onset of illness; and the remaining three successively; the mother was of the
4. Clustering. critical type with a poor prognosis; the daughter-in-law was
the mild type, the father and son were of the moderate type
Cluster disease refers to the occurrence of the same dis- with a good prognosis.
ease in one family, one unit, and there is an epidemiological
association between them. Familial aggregative morbidity is
Case 2 (Father) Case 1 (Mother) Case 4 (Son)
one of the most common forms. Due to individual differ-
ences in age, gender, health conditions, each cluster member
will have a different incubation period before disease onset,
Case 3 (Daughter-in-law)
clinical manifestations. Therefore, one familial member is
confirmed, the rest members with a close contact history
should have chest CT examination and viral RNA test as
early as possible. There is no obvious specificity in the CT 9.2.1 Case 1
manifestation of family agglomerative coronavirus pneumo-
nia, which can be manifested as multiple grinding glass den- A 72-year-old female patient with a disease-related exposure
sities with lung solidification, thickening of leaflet spacing history. Cough occurred 12 days ago. Fever occurred 5 days
and fibrosis of lung tissue in the peripheral zone of both ago and diarrhoea occurred 1 day ago. Admission body tem-
lungs. perature was 39 °C, with a maximum temperature of 39.6 °C
during the course of the illness. White blood cell count
was17.8  ×  109/L, lymphocyte count was 0.4  ×  109/L, and
R. Jiang (*) · X. Mo · Y. Li C-reactive protein was 72.88 mg/L. (Critical: oxygen satura-
Guangzhou Eighth People’s Hospital, Guangzhou Medical
University, Guangzhou, China

© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 163
J. Liu et al. (eds.), Atlas of Chest Imaging in COVID-19 Patients, https://doi.org/10.1007/978-981-16-1082-0_9
164 R. Jiang et al.

tion was 80–92%, D-2 aggregates was 3340  μg/L, lactate an exacerbation of the bilateral lung lesions with a “paving
dehydrogenase was 425 U/L). The patient underwent chest stone sign” and an increase in the number of bars (Fig. 9.1b, d,
CT scanned at day 13 and day 17 after onset of symptoms, f). A significant increase in the number and extent of bilateral
and was confirmed by CDC in Guangzhou. lung lesions was seen on day 13 versus day 17 CT (Fig. 9.1e, f).
CT scan showed multiple ground-glass opacities in bilateral
lungs on day 13 of onset (Fig. 9.1a, c, e). On day 17, CT showed

a b

c d

e f

Fig. 9.1  CT scan showed multiple ground-glass opacities in bilateral increase in the number of bars (b, d, f). A significant increase in the
lungs on day 13 of onset (a, c, e). On day 17, CT showed an exacerba- number and extent of bilateral lung lesions was seen on day 13 versus
tion of the bilateral lung lesions with a “paving stone sign” and an day 17 CT (e, f)
9  Imaging Analysis of Family Clustering COVID-19 165

9.2.2 Case 2 protein was <10  mg/L. (Normal: oxygen saturation was
94%, D-2 aggregates was 1520 μg/L). The patient was con-
A 73-year-old male patient with a history of family cluster- firmed by CDC in Guangzhou.
ing. Cough and fever occurred 2 days ago. Admission body CT of the chest on day 3 showed multiple ground-glass
temperature was 38.4  °C.  White blood cell count was opacities in bilateral lungs (Fig. 9.2a, b); CT of the chest on
3.59 × 109/L, lymphocyte count was 1.12 × 109/L, C-reactive day 6 showed multiple stripe shadows in the bilateral lobes

a b

c d

e f

Fig. 9.2  CT of the chest on day 3 showed multiple ground-glass opaci- tion visible (e white arrow). On day 22, CT showed a significant
ties in bilateral lungs (a, b); CT of the chest on day 6 showed multiple decrease in bilateral (f) lung lesions (g, h). Coronal position (day 9 vs.
stripe shadows in the bilateral lobes (c, d). Day 9 CT showed increased day 22 CT), significant reduction and partial disappearance of lesions
bilateral pulmonary stripe shadows, (e, f) with subpleural line forma- (i, j)
166 R. Jiang et al.

g h

i j

Fig. 9.2 (continued)

(Fig. 9.2c, d). Day 9 CT showed increased bilateral pulmo- 9.2.3 Case 3


nary stripe shadows with subpleural line formation visible
(Fig. 9.2e, f white arrow). On day 22, CT showed a signifi- A 35-year-old female patient with a history of family cluster-
cant decrease in bilateral lung lesions (Fig. 9.2g, h). Coronal ing. Admitted to hospital due to “pharyngeal discomfort for
position (day 9 vs. day 22 CT), significant reduction and par- 3 days”. The body temperature was 37  °C at the time of
tial disappearance of lesions (Fig. 9.2i, j). admission and there was no fever during the hospitalization.
9  Imaging Analysis of Family Clustering COVID-19 167

a b

c d

Fig. 9.3  Chest CT was not positive on days 5 and 13 (a–d)

White blood cell count was 5.64 × 109/L, lymphocyte count oxygen saturation was 97.9%). The patient was confirmed
was 2.07  ×  109/L, C-reactive protein was <10  g/L.  The by CDC in Guangzhou.
patient was confirmed by CDC in Guangzhou. CT of the chest on day 7 of the onset showed scattered patchy
Chest CT was not positive on days 5 and 13 (Fig. 9.3a–d). ground-glass opacity in bilateral lungs (Fig. 9.4a). CT on day 10
showed an increased range of intrapulmonary plaques in both
lungs (Fig. 9.4b). Day 13 CT showed an increased density of
9.2.4 Case 4 bilateral lung plaques compared to the anterior (Fig. 9.4c).
Day 17 CT showed a partial reduction in the extent of the
A 43-year-old male patient with a history of family clus- lesion (Fig. 9.4d).
tering. Admitted to hospital due to fever for 1 day and Day 21 CT showed a further reduction in the extent of
decreased sense of smell for 2 days. Admission body tem- bilateral lung lesions (Fig. 9.4e). Day 25 CT shows partial
perature was 38.5  °C.  White blood cell count was lesions that are more or less resorbed than before (Fig. 9.4f).
4.30  ×  109/L, lymphocyte count were1.76  ×  109/L, The coronal position is shown (day 17 vs. day 25 CT) and the
C-reactive protein was <10  mg/L. (Common type: blood lesion is clearly resorbed (Fig. 9.4g, h white arrow).
168 R. Jiang et al.

a b

c d

e f

Fig. 9.4  CT of the chest on day 7 of the onset showed scattered patchy the lesion (d). Day 21 CT showed a further reduction in the extent of
ground-glass opacity in bilateral lungs (a). CT on day 10 showed an bilateral lung lesions (e). Day 25 CT shows partial lesions that are more
increased range of intrapulmonary plaques in both lungs (b). Day 13 or less resorbed than before (f). The coronal position is shown (day 17
CT showed an increased density of bilateral lung plaques compared to vs. day 25 CT) and the lesion is clearly resorbed (g, h white arrow)
the anterior (c). Day 17 CT showed a partial reduction in the extent of
9  Imaging Analysis of Family Clustering COVID-19 169

g h

Fig. 9.4 (continued)

9.3 Family 2 9.3.2 Case 6

Families in this group: Daughters with first symptoms and par- A 43-year-old female patient with a history of family cluster-
ents with successive illnesses; daughters with mild symptoms ing. Admitted to hospital due to “Novel coronavirus nucleic
and parents with moderate symptoms with a good prognosis. acid positive found 1 day”. The body temperature was 36.3 °C
at the time of admission and there was no fever ­during the
Case 6 (Mother) Case 5 (Daughter) Case 7 (Father) hospitalization. White blood cell count was 4.44 × 109/L, lym-
phocyte count was 0.86  ×  109/L, C-reactive protein was
<10 mg/L. The patient was confirmed by CDC in Guangzhou.
9.3.1 Case 5 Chest CT on day 2 of admission was not significantly
positive (Fig. 9.6a).
A 19-year-old female patient with a disease-related expo- Day 5 CT scan shows ground-glass opacity in the left
sure history. Admitted to hospital due to fever for 3 days. lower lobe (Fig.  9.6b). Day 11 CT showed an increased
Maximum body temperature was 39.6 °C during the course extent of lesions in the lower left lobe of the lung (Fig. 9.6c).
of the disease. White blood cell count was 2.74  ×  109/L, Day 18 CT showed significant resorption of the left lower
lymphocyte count was 1.28 × 109/L, C-reactive protein was lobe of the lung (Fig. 9.6d). On day 11 compared with day
<10 mg/L. The patient was confirmed by CDC in Guangzhou. 18, the lesion range was reduced (Fig. 9.6e, f white arrows).
Chest CT was not positive on days 5 and 18 (Fig. 9.5a–d).
170 R. Jiang et al.

a b

c d

Fig. 9.5  Chest CT was not positive on days 5 and 18 (a–d)


9  Imaging Analysis of Family Clustering COVID-19 171

a b

c d

e f

Fig. 9.6  Chest CT on day 2 of admission was not significantly positive lobe of the lung (c). Day 18 CT showed significant resorption of the left
(a). Day 5 CT scan shows ground-glass opacity in the left lower lobe lower lobe of the lung (d). On day 11 compared with day 18, the lesion
(b). Day 11 CT showed an increased extent of lesions in the lower left range was reduced (e, f white arrows)
172 R. Jiang et al.

9.3.3 Case 7 CT on day 5 of the onset showed a ground-glass nodules


in the right lower lobe, with unclear boundary (Fig.  9.7a
A 48-year-old female patient with a history of family cluster- empty arrow). On day 9, CT showed an increase in plaque
ing. Admitted to hospital due to “Fever for 4 days with cough grinding ground-glass nodules in the lower lobe of the right
and sputum for 3 days”. The body temperature was 37.8 °C lung with a thickened central lobe structure and an increased
at the time of admission and there was no fever during the lesion extent (Fig.  9.7b1, b2 empty arrows). Day 21 CT
hospitalization. White blood cell count was 4.59  ×  109/L, showed a decrease in right lobe lesions (Fig. 9.7c).
lymphocyte count was 2.10 × 109/L, C-reactive protein was Day 9 vs. day 21 CT, with reduced lesion extent and
<10 mg/L. The patient was confirmed by CDC in Guangzhou. increased density (Fig. 9.7d, e white arrows).

a b1

b2 c

Fig. 9.7  CT on day 5 of the onset showed a ground-glass nodules in an increased lesion extent (b1, b2 empty arrows). Day 21 CT showed a
the right lower lobe, with unclear boundary (a empty arrow). On day 9, decrease in right lobe lesions (c). Day 9 vs. day 21 CT, with reduced
CT showed an increase in plaque grinding ground-glass nodules in the lesion extent and increased density (d, e white arrows)
lower lobe of the right lung with a thickened central lobe structure and
9  Imaging Analysis of Family Clustering COVID-19 173

d e

Fig. 9.7 (continued)

9.4 Family 3 breath for 9 days after activity, exacerbated for 3 days”. The
body temperature on admission was 37.2 °C and there was
Families in this group: the older brother first developed no fever during the hospital stay. White blood cell count was
symptoms and his mother and brother successively; all three 10.03 × 109/L, lymphocyte count was 0.55 × 109/L, C-reactive
were seriously ill and had a poor prognosis. protein was 124.1 mg/L. (Critical type: blood oxygen satura-
tion was <90%, plasma D-dimer was >10  mg/L, lactate
dehydrogenase was 649 U/L) The patient was confirmed by
Case 10 (Mother) Case 8 (The older brother) Case 9 (Brother)
CDC in Guangzhou.
A diffuse patchy, slightly dense, “white lung-like” mani-
9.4.1 Case 8 festation was seen in both lungs on the 10th day of illness on
a paraplegic chest piece (Fig. 9.8a).
A 64-year-old male patient with a disease-related exposure On day 11, the bilateral lung lesions were smaller in
history. Admitted to the hospital with “fever, shortness of extent and less dense than before (Fig. 9.8b).
174 R. Jiang et al.

a b

Fig. 9.8  A diffuse patchy, slightly dense, “white lung-like” manifestation was seen in both lungs on the 10th day of illness on a paraplegic chest
piece (a). On day 11, the bilateral lung lesions were smaller in extent and less dense than before (b)

9.4.2 Case 9 9.4.3 Case 10

A 58-year-old male patient was admitted to the hospital for A 84-year-old female patient admitted to hospital with
“9 days of contact with a suspected case of novel coronavi- “cough and chest tightness for 2 days” with a family history
rus pneumonia” with a body temperature of 38  °C on of gathering. The temperature on admission was 36.4  °C,
admission and a maximum temperature of 38.4 °C during with a maximum temperature of 38 °C during the course of
the course of the illness. White blood cell count was the illness. White blood cell count was 4.75 × 109/L, lym-
6.69 × 109/L, lymphocyte count was 2.14 × 109/L, C-reactive phocyte count was 1.54  ×  109/L, C-reactive protein was
protein was 25.1  mg/L. (Critical: oxygen saturation was 70.2  mg/L. (Critical type: blood oxygen saturation was
86–90%). The patient was confirmed by CDC in Guangzhou. <90%, plasma D-dimer was 1.1 mg/L) The patient was con-
CT of the chest on day 3 of hospital admission showed firmed by CDC in Guangzhou.
scattered bilateral lung dense in the form of a patchy milli- CT of the chest on day 3 of the onset showed scattered,
glass (Fig. 9.9a). On day 6, CT showed multiple patches and patchy, ground-glass opacity of both lungs (Fig. 9.10a, a1).
bars in both lungs, with a larger area and more lesions CT on day 6 showed an increased range of bilateral lung
(Fig. 9.9b). lesions (Fig. 9.10b, b1). Diffuse densities of both lungs on
On day 9, CT showed a significant increase in lesions the paraplegic chest piece on day 11 with a “white lung”
with thickening of the lobule interval and intrafollicular presentation (Fig. 9.10c).
interval (Fig. 9.9c, d). On day 3 compared with day 9 CT, The range and density of bilateral lung lesions on days 19,
there was a significant increase in lesions, an increase in 21, and 26 of the onset were smaller and less dense than
extent, and a decrease in partial lung volume (Fig. 9.9e, f). before (Fig. 9.10d–f).
9  Imaging Analysis of Family Clustering COVID-19 175

a b

c d

e f

Fig. 9.9  CT of the chest on day 3 of hospital admission showed scat- lesions with thickening of the lobule interval and intrafollicular interval
tered bilateral lung dense in the form of a patchy milliglass (a). On day (c, d). On day 3 compared with day 9 CT, there was a significant
6, CT showed multiple patches and bars in both lungs, with a larger area increase in lesions, an increase in extent, and a decrease in partial lung
and more lesions (b). On day 9, CT showed a significant increase in volume (e, f)
176 R. Jiang et al.

a b

a1 b1

c d

Fig. 9.10  CT of the chest on day 3 of the onset showed scattered, patchy, lungs on the paraplegic chest piece on day 11 with a “white lung” presen-
ground-glass opacity of both lungs (a, a1). CT on day 6 showed an tation (c). The range and density of bilateral lung lesions on days 19, 21,
increased range of bilateral lung lesions (b, b1). Diffuse densities of both and 26 of the onset were smaller and less dense than before (d–f)
9  Imaging Analysis of Family Clustering COVID-19 177

e f

Fig. 9.10 (continued)

disease control and prevention. JAMA. 2020;323(13):1239–42.


References https://doi.org/10.1001/jama.2020.2648. PMID: 32091533
3. Zhuang YL, et  al. Analysis on the cluster epidemic of corona-
1. Wang X, Zhou Q, He Y, et al. Nosocomial outbreak of COVID-19 virus disease 2019  in Guangdong Province. Zhonghua Yu Fang
pneumonia in Wuhan, China. Eur Respir J. 2020;55(6):2000544. Yi Xue Za Zhi. 2020;54(7):720–5. https://doi.org/10.3760/
https://doi.org/10.1183/13993003.00544-­2020. Print 2020 Jun. cma.j.cn112150-­20200326-­00446.
PMID: 32366488 4. Guan Q, Liu M, Zhuang YJ, Yuan Y.  Epidemiological investiga-
2. Wu Z, McGoogan JM.  Characteristics of and important lessons tion of a family clustering of COVID-19. Zhonghua Liu Xing
from the coronavirus disease 2019 (COVID-19) outbreak in China. Bing Xue Za Zhi. 2020;41(5):629–33. https://doi.org/10.3760/
Summary of a report of 72 314 cases from the Chinese center for cma.j.cn112338-­20200223-­00152.
Residual CT Features in Recovery Stage
of COVID-19 Pneumonia 10
Yanhong Yang, Lieguang Zhang, Haiyan Shi,
and Sufang Tian

10.1 Introduction 10.2 Case 1 (Fig. 10.1a–f )

CT scan is not only used to initially assess the degree of lung A 65-year-old male was admitted with fever for 11 days,
involvement, but also to determine complications, guide treat- accompanied by diarrhea for 5 days and short-breathed for 3
ment plans, and monitor the progression and changes of pneu- days. He had no exposure to infected patient or epidemic
monia, especially patients with functional respiratory disorder area. The body temperature at admission was 39.2 °C. White
and/or hypoxemia after recovery from COVID-19 [1–5]. blood cell count, neutrophil count, lymphocyte count, and
There are many published researches focused on the the C-reactive protein were 6.74  ×  109/L, 5.82  ×  109/L,
dynamic changes of chest CT, Liu N. et  al. showed that the 0.67 × 109/L, and 68.0 mg/L, respectively. The patient was
occurrence rate of ground-glass opacity, crazy paving pattern, laboratory confirmed by novel coronavirus nucleic acid
pleural thickening in severe and critical group is higher [6]. throat swab test in Guangzhou CDC. Chest CT examination
Meanwhile, some researchers found that more than half of was performed on 213 days after onset of symptoms
patients still had abnormal imaging findings on chest CT such (Fig. 10.1a–f).
as linear opacities, especially in severe or critical patients [7, 8]. On 213 days after onset of symptoms, chest CT images
According to the follow-up data of COVID-19 patients (Fig.  10.1a–f) showed patchy ground-glass opacities with
treated in Guangzhou Eighth People’s Hospital, we found that thickening of the interlobular septa and linear opacities in
ground-glass opacities and linear opacities could be seen in bilateral lung.
some patients although they had recovered and discharged
from hospital, and others showed negative results on chest CT.

Y. Yang (*) · L. Zhang · H. Shi


Guangzhou Eighth People’s Hospital, Guangzhou Medical
University, Guangzhou, China
S. Tian
Zhongnan Hospital of Wuhan University, Wuhan, China

© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 179
J. Liu et al. (eds.), Atlas of Chest Imaging in COVID-19 Patients, https://doi.org/10.1007/978-981-16-1082-0_10
180 Y. Yang et al.

a b

c d

e f

Fig. 10.1  On 213 days after onset of symptoms, chest CT images (a–f) showed patchy ground-glass opacities with thickening of the interlobular
septa and linear opacities in bilateral lung
10  Residual CT Features in Recovery Stage of COVID-19 Pneumonia 181

10.3 Case 2 (Fig. 10.2a–f ) and 36.12 mg/L, respectively. The patient was laboratory con-
firmed by novel coronavirus nucleic acid throat swab test in
A 54-year-old female was admitted with fever for 6 days. He Guangzhou CDC. Chest CT examination was performed on
had exposed to confirmed cases with novel coronavirus pneu- 194 days after onset of symptoms (Fig. 10.2a–f).
monia. The body temperature at admission was 39.9 °C. White On 194 days after onset of symptoms, chest CT images
blood cell count, neutrophil count, lymphocyte count, and the (Fig. 10.2a–f) showed linear opacities in the middle lobe of
C-reactive protein were 5.4 × 109/L, 3.64 × 109/L, 1.49 × 109/L, right lung.

a b

c d

e f

Fig. 10.2  On 194 days after onset of symptoms, chest CT images (a–f) showed linear opacities in the middle lobe of right lung
182 Y. Yang et al.

10.4 Case 3 (Fig. 10.3a–f ) count, neutrophil count, lymphocyte count, and the C-reactive
protein were 4.59  ×  109/L, 1.99  ×  109/L, 2.1  ×  109/L, and
A 48-year-old male was admitted with fever for 4 days, <10 mg/L, respectively. The patient was laboratory confirmed
accompanied by cough and expectoration. He had exposed to by novel coronavirus nucleic acid throat swab test in
confirmed cases with novel coronavirus pneumonia. The Guangzhou CDC. Chest CT examination was performed on
body temperature at admission was 37.8 °C. White blood cell 198 days after onset of symptoms (Fig. 10.3a–f).

a b

c
d

e f

Fig. 10.3  On 198 days after onset of symptoms, chest CT images (a–f) showed patchy ground-glass opacities in the upper lobe of right lung (b, e, f)
10  Residual CT Features in Recovery Stage of COVID-19 Pneumonia 183

On 198 days after onset of symptoms, chest CT images body temperature at admission was 37.9 °C. White blood cell
(Fig. 10.3a–f) showed patchy ground-glass opacities in the count, neutrophil count, lymphocyte count, and the C-reactive
upper lobe of right lung (Fig. 10.3b, e, f). protein were 5.56  ×  109/L, 3.50  ×  109/L, 1.75  ×  109/L, and
35.36  mg/L, respectively. The patient was laboratory con-
firmed by novel coronavirus nucleic acid throat swab test in
10.5 Case 4 (Fig. 10.4a–f ) Guangzhou CDC. Chest CT examination was performed on
195 days after onset of symptoms (Fig. 10.4a–f).
A 65-year-old male was admitted with fever for 8 days. He On 195 days after onset of symptoms, chest CT images
had no exposure to infected patient or epidemic area. The (Fig. 10.4a–f) showed normal in bilateral lung.

a b

c d

e
f

Fig. 10.4  On 195 days after onset of symptoms, chest CT images (a–f) showed normal in bilateral lung
184 Y. Yang et al.

10.6 Case 5 (Fig. 10.5a–e) phil count, lymphocyte count, and the C-reactive protein
were 6.28  ×  109/L, 5.35  ×  109/L, 0.77  ×  109/L, and
An 81-year-old male was admitted with recurrent fever 60.5 mg/L, respectively. The patient was laboratory con-
for 10 days, accompanied by chills, headache, dizziness, firmed by novel coronavirus nucleic acid throat swab test
and muscle soreness. He had exposed to confirmed cases in Guangzhou CDC.  Chest CT examination was per-
with novel coronavirus pneumonia. The body temperature formed on 21 days after onset of symptoms
at admission was 39 °C. White blood cell count, neutro- (Fig. 10.5a–e).

a b

c d

Fig. 10.5  On 21 days after onset of symptoms, chest CT images (a–e) showed linear opacities in bilateral lung
10  Residual CT Features in Recovery Stage of COVID-19 Pneumonia 185

On 21 days after onset of symptoms, chest CT images body temperature at admission was 38.6  °C.  White blood
(Fig. 10.4a–e) showed linear opacities in bilateral lung. cell count, neutrophil count, lymphocyte count, and the
C-reactive protein were 3.05  ×  109/L, 2.16  ×  109/L,
0.56 × 109/L, and <10 mg/L. The patient was laboratory con-
10.7 Case 6 (Fig. 10.6a–e) firmed by novel coronavirus nucleic acid throat swab test in
Guangzhou CDC. Chest CT examination was performed on
A 62-year-old male was admitted with fever for 5 days, 29 days after onset of symptoms (Fig. 10.6a–e).
accompanied by chills and muscle soreness. He had exposed On 29 days after onset of symptoms, chest CT images
to confirmed cases with novel coronavirus pneumonia. The (Fig. 10.4a–e) showed linear opacities in bilateral lung.

a b

c d e

Fig. 10.6  On 29 days after onset of symptoms, chest CT images (a–e) showed linear opacities in bilateral lung
186 Y. Yang et al.

References 4. Lu X, Gong W, Peng Z, et al. High resolution CT imaging dynamic


follow-up study of novel coronavirus pneumonia. Front Med.
2020;7:168. https://doi.org/10.3389/fmed.2020.00168.
1. Rubin GD, Ryerson CJ, Haramati LB, et  al. The role of chest
5. Vernuccio F, Giambelluca D, Cannella R, et al. Radiographic and
imaging in patient management during the COVID-19 pan-
chest CT imaging presentation and follow-up of COVID-19 pneu-
demic: a multinational consensus statement from the Fleischner
monia: a multicenter experience from an endemic area. Emerg
Society. Chest. 2020;158:106–16. https://doi.org/10.1016/j.
Radiol. 2020;11:1–10.
chest.2020.04.003.
6. Liu N, He G, Yang X, et al. Dynamic changes of chest CT follow-
2. Tabatabaei SMH, Talari H, Moghaddas F, Rajebi H.  Computed
­up in coronavirus disease-19 (COVID-19) pneumonia: relationship
tomographic features and short-term prognosis of coronavirus
to clinical typing. BMC Med Imaging. 2020;20(1):92. https://doi.
disease 2019 (COVID-19) pneumonia: a single-center study from
org/10.1186/s12880-­020-­00491-­2.
Kashan, Iran. Radiol Cardiothor Imaging. 2020;2(2):e200130.
7. Li M, Lei P, Zeng B, et al. Coronavirus disease (COVID-19): spec-
https://doi.org/10.1148/ryct.2020200130.
trum of CT findings and temporal progression of the disease. Acad
3. Francone M, Iafrate F, Masci GM, et  al. Chest CT score in

Radiol. 2020;27:603–8. https://doi.org/10.1016/j.acra.2020.03.003.
COVID-­19 patients: correlation with disease severity and short-term
8. Huang Y, Yan Tan C, Wu J, et al. Impact of coronavirus disease 2019
prognosis. Eur Radiol. 2020;4:1–6817. https://doi.org/10.1007/
on pulmonary function in early convalescence phase. Respir Res.
s00330-­020-­07033-­y.
2020;21(1):163. https://doi.org/10.1186/s12931-­020-­01429-­6.
CT Features and Pathological Analysis
of COVID-19 Death 11
Jing Qu, Li Liang, Meiyan Liao, and Ying Liu

11.1 Introduction Guangzhou CDC. Chest CT examination was performed on


day 1 (6 days after the onset of symptoms) of admission.
SARS-CoV-2 has claimed the lives of 1 million people. The Bedside chest radiographs were successively taken on day 8
main cause of death is due to multiple organ failure, diffuse (13 days after the onset of symptoms), day 15 (20 days after
intravascular hemorrhage, septic shock, and other serious the onset of symptoms), and day 19 (24 days after the onset
complications. There was only one death case in Guangzhou of symptoms) of admission. Postmortem pathology was per-
Eighth People’s Hospital. To show the typical imaging fea- formed on day 33 (38 days after the onset of symptoms) of
tures of death cases, we also include another death case in admission, as shown in Fig.  11.1a–l. (Thanks to Professor
Central South University Hospital of Wuhan University. Ding Yanqing and Professor Liang Li, Department of
The hyaline membrane is the end-stage manifestation of Pathology, Southern Hospital, Southern Medical University,
COVID-19, which is formed by diffuse alveolar injury with for providing the pathological pictures of this case.)
fibromyxoid exudate in both lungs, with significant alveolar On day 1 of admission, chest CT images showed that mul-
epithelial cell detachment. It does not occur in all critically tiple ground-glass opacities with thickened interlobular sep-
ill or dead patients. However, pulmonary edema, protein tum were found in the bilateral lung, which showed a
exudation, pulmonary interstitial thickening, and inflamma- “crazy-paving pattern” (Fig. 11.1a–d).
tory cell infiltration in the alveolar cavity are the common Bedside chest radiographs were successively taken on
basic pathological changes [1–3]. day 8, day 15, and day 19 of admission, which showed that
the lesions in bilateral lungs of the patient were gradually
aggravated and showed “white lung” at last (Fig. 11.1e–h).
11.2 Case 1 (Fig. 11.1a–l) On day 33 of admission, the patient died due to multiple
organ dysfunction syndrome (MODS) and dessiminated intra-
An 82-year-old male was admitted to the hospital with fever vascular coagulation (DIC). At low magnification (Fig. 11.1i,
for 5 days. The body temperature at admission was j), consolidation and interstitial fibrosis were evidently pres-
37.4 °C. Laboratory examination: white blood cell count in ent. Alveolar septum widened and fibrous tissue proliferated,
peripheral blood was 4.57  ×  109/L, lymphocyte count was and a small amount of fibrin-like exudate was present between
0.45 × 109/L, C-reactive protein was 36.7 mg/L, and oxygen- alveoli. The type II alveolar epithelium was proliferated and
ation index was 245 mmHg. The patient was laboratory con- detached in the alveolar cavity, which was intermixed with the
firmed by novel coronavirus nucleic acid throat swab test in proliferated macrophages some alveolar tissues were orga-
nized. There was a small amount of chronic inflammatory cell
infiltrated in the pulmonary interstitium with focal hemor-
rhage. And no clear bacterial, fungal, or viral inclusions were
J. Qu (*) · Y. Liu observed.
Guangzhou Eighth People’s Hospital, Guangzhou Medical
University, Guangzhou, China
At high magnification (Fig. 11.1k, l), alveolar septum sig-
nificantly widened, and fibrous tissue proliferated. The type
L. Liang
Nanfang Hospital, Southern Medical University, Guangzhou,
II alveolar epithelium was proliferated and detached in the
China alveolar cavity, which was intermixed with the proliferated
M. Liao
macrophages. There was a small amount of chronic inflam-
Zhongnan Hospital of Wuhan University, Wuhan, China matory cell infiltrated in the pulmonary interstitium.

© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 187
J. Liu et al. (eds.), Atlas of Chest Imaging in COVID-19 Patients, https://doi.org/10.1007/978-981-16-1082-0_11
188 J. Qu et al.

a b

c d

Fig. 11.1  On day 1 of admission, chest CT images showed that mul- erated and detached in the alveolar cavity, which was intermixed with
tiple ground-glass opacities with thickened interlobular septum were the proliferated macrophages. And partial alveolar was organized.
found in the bilateral lung, which showed a “crazy-paving pattern” (a– There was a small amount of chronic inflammatory cell infiltrated in the
d). Bedside chest radiographs were successively taken on day 8, day 15, pulmonary interstitium with focal hemorrhage. And no clear bacterial,
and day 19 of admission, which showed that the lesions in bilateral fungal, or viral inclusions were observed. At high magnification (k, l),
lungs of the patient were gradually aggravated and showed “white alveolar septum significantly widened and fibrous tissue proliferated.
lung” at last (e–h). On day 33 of admission, the patient died due to The type II alveolar epithelium was proliferated and detached in the
MODS and DIC. At low magnification (i, j), consolidation and intersti- alveolar cavity, which was intermixed with the proliferated macro-
tial fibrosis were evidently present. Alveolar septum widened and phages. There was a small amount of chronic inflammatory cell infil-
fibrous tissue proliferated, and a small amount of fibrin-like exudate trated in the pulmonary interstitium
was present between alveoli. The type II alveolar epithelium was prolif-
11  CT Features and Pathological Analysis of COVID-19 Death 189

e f

g h

Fig. 11.1 (continued)
190 J. Qu et al.

i j

k l

Fig. 11.1 (continued)
11  CT Features and Pathological Analysis of COVID-19 Death 191

11.3 Case 2 (Fig. 11.2a–h) with local consolidation and thickening of interlobular


and intralobular septa, formed a “crazy-paving pattern”
A 74-year-old male was laboratory confirmed by novel coro- (Fig.  11.2a). There was a little pleural effusion
navirus nucleic acid throat swab test in Wuhan CDC.  The (Fig. 11.2a–f).
highest temperature in the course of the disease was The pathological images showed a pink hyaline mem-
38.2 °C. The patient was diagnosed as severe on day 3 and brane attached to the alveolar wall (Fig. 11.2g). The patho-
died on day 7 of admission. (Thanks to Professor Liao logical images showed alveolar injury: some alveolar
Meiyan of the Department of Radiology and Professor Tian epithelium was detached, some type II alveolar epithelium
Sufang of the Department of Pathology, Central South was proliferated, and cellulose exudate was present in the
Hospital, Wuhan University, for their case.) upper right corner. A few inflammatory cells infiltrated the
Chest CT images showed multiple ground-glass opaci- pulmonary interstitium (Fig. 11.2h).
ties in both lungs, especially in the right lung, which,

a b

c d

Fig. 11.2  Chest CT images showed multiple ground-glass opacities in wall (g). The pathological images showed alveolar injury: some alveo-
both lungs, especially in the right lung, which, with local consolidation lar epithelium was detached, some type II alveolar epithelium was pro-
and thickening of interlobular and intralobular septa, formed a “crazy-­ liferated, and cellulose exudate was present in the upper right corner. A
paving pattern” (a). There was a little pleural effusion (a–f). The patho- few inflammatory cells infiltrated the pulmonary interstitium (h)
logical images showed a pink hyaline membrane attached to the alveolar
192 J. Qu et al.

e f

g h

Fig. 11.2 (continued)

References 2. Xu Z, Shi L, Wang Y, et  al. Pathological findings of COVID-19


associated with acute respiratory distress syndrome. Lancet Respir
Med. 2020; https://doi.org/10.1016/S2213-­2600(20)30076-­X.
1. Tian S, Hu W, Niu L, et  al. Pulmonary pathology of early-phase
3. Joob B, Wiwanitkit V.  Pulmonary pathology of early phase 2019
2019 novel coronavirus (COVID-19) pneumonia in two patients
novel coronavirus pneumonia. J Thorac Oncol. 2020;15(5):e67.
with lung cancer. J Thorac Oncol. 2020; https://doi.org/10.1016/j.
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