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Received: 2015.12.04
Accepted: 2016.01.12
Published: 2016.08.08
2367 2 3 31
Thin-Section Computed Tomography
Manifestations During Convalescence and Long-
Term Follow-Up of Patients with Severe Acute
Respiratory Syndrome (SARS)
ABC 1 Xiaohua Wu
CD 2 Dawei Dong
DE 1 Daqing Ma
Corresponding Author: Daqing Ma, e-mail: cjr.madaqing@vip.163.com
Source of support: Departmental sources
Background: SARS is not only an acute disease, but also leads to long-term impaired lung diffusing capacity in some survi-
vors. However, there is a paucity of data regarding long-term CT findings in survivors after SARS. The aim of
this study was to assess the changes in lung function and lung thin-section computed tomography (CT) fea-
tures in patients recovering from severe acute respiratory syndrome (SARS), especially the dynamic changes in
ground-glass opacity (GGO).
Material/Methods: Clinical and radiological data from 11 patients with SARS were collected. The serial follow-up thin-section CTs
were evaluated at 3, 6, and 84 months after SARS presentation. The distribution and predominant thin-sec-
tion CT findings of lesions were evaluated.
Results: The extent of the lesions on the CT scans of the 11 patients decreased at 6 and 84 months compared to 3
months. The number of segments involved on 84-month follow-up CTs was less than those at 6 months (P<0.05).
The predominant thin-section CT manifestation at 84 months (intralobular and interlobular septal thickening)
was different than that at 6 months, at which GGO was predominant.
Conclusions: During convalescence after SARS, GGO and intralobular and interlobular septal thickening were the main thin-
section CT manifestation. Intralobular and interlobular septal thickening predominated over GGO at 84 months.
MeSH Keywords: Pneumonia, Viral • Severe Acute Respiratory Syndrome • Tomography Scanners, X-Ray Computed
Full-text PDF: http://www.medscimonit.com/abstract/index/idArt/896985
Authors’ Contribution:
Study Design A
Data Collection B
Statistical Analysis C
Data Interpretation D
Manuscript Preparation E
Literature Search F
Funds Collection G
1 Department of Radiology, Beijng Friendship Hospital, Capital Medical University,
Beijing, P.R. China
2 Department of Radiology, Beijng Xiaotangshan Hospital, Beijing, P.R. China
e-ISSN 1643-3750
© Med Sci Monit, 2016; 22: 2793-2799
DOI: 10.12659/MSM.896985
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Background
Severe acute respiratory syndrome (SARS) is an emergent
infectious disease that was epidemic in 2002 and 2003 [1].
Between November 2002 and July 2003, an outbreak of SARS
in southern China infected about 8000 people and led to 774
recorded deaths, mostly in Hong Kong [1]. Within weeks, SARS
spread from Hong Kong to 37 countries [2]. A novel corona-
virus (SARS-CoV) is responsible for SARS. The coronavirus re-
sponsible for Middle East Respiratory Syndrome (MERS-CoV)
is similar to SARS-CoV. A better understanding of the features
of SARS-CoV would help to guide control measures and treat-
ment for similar diseases, such as MERS-CoV [3,4].
Lung injury caused by SARS-CoV is one of the main clinical
manifestations and directly affects prognosis. Imaging plays
an important role in the diagnosis and evaluation of patients
with SARS. Thin-section computed tomography (CT) can show
pulmonary abnormalities in patients with normal findings on
plain X-ray and is useful in depicting the patterns and extent
of the abnormalities [5–8]. During the acute phase of SARS,
the more distinctive radiographic features include the pre-
dominant involvement of lung periphery and lower zone, and
the absence of cavitation, hilar lymphadenopathy, and pleu-
ral effusion [9,10]. Radiographic progression from unilateral
focal lesion to either multifocal or bilateral involvement dur-
ing the second phase of the disease, followed by radiographic
improvement with treatment, are commonly observed [9,10].
SARS is not only an acute disease, but also leads to long-
term impaired lung diffusing capacity in about 24% of sur-
vivors [11], resulting in significantly lower exercise tolerance
compared with the age-matched general population [11–13].
Another study suggested that the lung function impairment
might not be related to the disease itself, but rather to extra-
pulmonary muscle weakness [14]. Nevertheless, 75% of SARS
survivors still show lung abnormalities on thin-section CT 5
years after their illness onset [14].
However, there is a paucity of data regarding long-term CT find-
ings in survivors after SARS. Therefore, the aim of the pres-
ent study was to assess the changes in lung function and lung
thin-section CT features in patients recovering from SARS, es-
pecially the dynamic changes in ground-glass opacity (GGO).
Material and Methods
Patients
Eleven patients who had been discharged after treatment
for SARS as inpatients between February and June 2003 at
Beijing Friendship Hospital were followed up at 3, 6, and 84
months using thin-section CT and were included in the present
study. The diagnosis of SARS was based on the World Health
Organization criteria [15].
This study received Ethics Committee approval from Beijing
Friendship Hospital affiliated to Capital Medical University
(Approval ID: 2015-P2-076-01). The committees waived the
need for individual consent because of the retrospective na-
ture of the study.
CT scans
The CT examinations were performed with an 8-row multi
-
detector CT scanner (High Speed Ultra; GE Medical Systems,
Milwaukee, WI, USA), and a 64-row multidetector CT scanner
(LightSpeed Ultra; GE Medical Systems, Milwaukee, WI, USA)
using the following parameters: 120 kVp, 150 mA, 5-mm col-
limation, 1.35:1 pitch, and reconstruction matrix of 512×512.
The subjects were scanned in a supine position during breath-
holding at full inspiration. Thin-section CT images were re-
constructed with 0.625-mm or 1.25-mm collimation with a
high spatial frequency algorithm or standard algorithm and
then sent to the workstation (ADW 4.2; GE Medical Systems,
Milwaukee, WI, USA) for analyzing. Thin-section CT images
were evaluated using a lung window, with a window level of
–600 HU and window width of 1500 HU. The soft-tissue win-
dow was not evaluated.
Image interpretation
All thin-section CT images were reviewed by 2 radiologists. The
radiologists were aware of the diagnosis of SARS. For all scans,
the radiologists were blinded to the names of the patients and
the length of time since onset, but they were aware of which
images belonged to the same patient. A consensus had to be
reached between the 2 radiologists about the abnormalities.
Discrepancies were solved by discussion.
The radiologists determined the extent of the following thin-
section CT abnormalities: ground-glass opacity, consolidation,
reticular pattern, patchy decreased attenuation, and subpleu-
ral line, in accordance with the standard morphologic descrip-
tors based on the Fleischner Society Nomenclature Committee
recommendations [16] and other studies [17,18]. The evalua-
tion of the extent of lung involvement was based on the seg-
ments of the lung anatomy: 10 segments in the right lung and
10 segments in the left lung (2 segments were considered in
the apicoposterius segment left upper lobe and 2 segments
were considered in the inferior front segment of the left low-
er lobe). The following rules were used to evaluate the lobe
involvement: if more than half of the segment on the biggest
scope of lesion level on axial thin-section CT was involved,
then the segment (1 point) was recorded as being involved;
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if no more than half of the segment was involved, then 0.5
point was recorded.
To evaluate the distribution of the lesion, it was also classi-
fied into 3 categories: 1) subpleural and/or peribronchovascu-
lar, 2) diffuse, or 3) irregular. In addition, each CT was divided
into 3 categories: 1) anterior, 2) posterior, or 3) anterior and
posterior. Finally, for every CT scan, the radiologists were re-
quired to generalize the main CT manifestation: 1) GGO pre-
dominant, or 2) fine reticulation predominant.
Pulmonary function test (PFT)
The PFT of the patients was classified into mild, moderate, or
serious. We evaluated lung volumes (total lung capacity [TLC],
vital capacity [VC], residual volume [RV], functional residual
capacity [FRC] using the nitrogen washout method), spirometry
(forced vital capacity [FVC], forced expiratory volume in 1 sec-
ond [FEV1], FEV1/FVC ratio), and surface area for gas exchange
(diffusion capacity adjusted for hemoglobin [DLCO]). The DLCO
was determined using the single-breath carbon monoxide tech-
nique and an infrared analyzer. FEV1/expected% of <30%, 30–
50%, 50–80%, and >80% were regarded as extremely serious,
serious, moderate, and mild, respectively. DLCO values <80%
of predicted were regarded as being impaired.
Statistical analysis
Descriptive statistics are presented. Continuous data are pre-
sented as means ± standard deviation (SD). Categorical data
are presented as frequencies. SPSS 16.0 (IBM, Armonk, NY,
USA) was used for statistical analysis.
Case
number Gender Age at
onset
3 months 6 months 84 months
Predominant
HRCT findings
Segments
involved
Predominant
HRCT findings
Segments
involved
Predominant
HRCT findings
Segments
involved PFT
1 F 30 GGO 15
Reticulation
and
interlobular
thickening
15
Reticulation
and interlobular
thickening
15 Mild
2 M 35 GGO 3 GGO 2 GGO 1 Mild
3 M 54
Consolidation
and GGO 8 GGO 6
Reticulation
and interlobular
thickening
4 N
4 F 38 Diffuse GGO 9 GGO 3
Reticulation
and interlobular
thickening
3 Mild
5 F 42
Consolidation
and GGO 13
Reticulation
and
interlobular
thickening
7
Reticulation
and interlobular
thickening
5 Mild
6 F 32 – – GGO 14
Reticulation
and interlobular
thickening
11.5 Mild
7 M 31 – – GGO 18
Reticulation
and interlobular
thickening
9.5 Mild
8 F 31 – –
Reticulation
and
interlobular
thickening
5
Reticulation
and interlobular
thickening
3.5 Mild
9 F 40 – – GGO 9
Reticulation
and interlobular
thickening
6.5
Moderate
10 F 48 – – GGO 18 GGO 16 Mild
11 F 36 – – GGO 9 Normal 0 N
Table 1. Characteristics of the patients.
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CT during convalescence after SARS
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Results
Characteristics of the patients
Eleven patients (8 females and 3 males; age range: 30–54 years,
mean age: 38.6 years) met the selection criteria. Table 1 pres-
ents the demographic data and changes in lung function and
lung radiographic features of the 11 patients during follow-
up. All of the 11 patients were healthy before developing SARS
and none were smokers. In acute phase, glucocorticoid was
used in all 11 patients (methylprednisolone; the biggest dose
was 840 mg/d, mean duration 9.5 days, and after improving
for 2 or 3 days, methylprednisolone dose was decreased). All
patients were still alive during the study period. Twenty-seven
CT scans were evaluated. At 84 months, 5 patients were still
experiencing persistent dyspnea, 4 had cough, 2 had sputum
production, and 2 experienced all 3 symptoms. The mean time
from discharge to the first follow-up was 3 months (range, 2
to 4 months).
Thin-section CT findings
Table 2 presents the thin-section CT findings. All 11 patients
underwent CT scans at 6- and 84-month follow-up. Multiple
lobes or segments were involved in all 11 cases. Among them,
48 segments (average of 10 segments per patient) were in-
volved at 3 months, 106 segments (average of 9.6 per case)
were involved at 6 months, and 75 segments (average of
6.8 per case) were involved at 84 months. At 3 months, as
the predominant thin-section CT feature, 2 patients (40.0%)
showed GGO (Figure 1) and 3 showed consolidation and GGO
(60.0%) (Figure 2). At 6 months, as the predominant thin-sec-
tion CT feature, 3 patients (27.3%) showed reticulation and
interlobular thickening (Figure 3) and 8 (72.7%) showed GGO.
At 84 months, as the predominant thin-section CT feature, 1
patient (9.1%) had no lung abnormality, 8 patients (72.7%)
showed reticulation and interlobular thickening, and 2 (18.2%)
showed GGO. Traction bronchiectasis was found in 3 patients
(Figure 3), while patchy decreased attenuation was found in 1
patient (Figure 1). Traction bronchiectasis was found at 6- and
84-month thin-section CT, and patchy decreased attenuation
was found at 3-, 6-, and 84-month thin-section CT.
Pulmonary function test
The PFT results of the 11 patients at 84 months are present-
ed in Table 1. Two patients (18%) had a normal PFT. Nine pa-
tients (81.8%) had a low DLCO. Eight patients (72.7%) had
mild lung function damage, and 1 (9.1%) had moderate lung
function damage.
Trends in changes in predominant thin-section CT findings
over time
Table 2 shows that the predominant CT findings in SARS sur-
vivors shift from a predominance of the GGO feature at 3
(100.0%) and 6 (72.7%) months to the predominance of re-
ticulation and interlobular thickening at 84 months (72.7%).
Figuress 1–3 present typical thin-section CT imaging at 3, 6,
and 84 months, respectively.
CT findings 3 months (n=5) 6 months (n=11) 84 months (n=11)
GGO 5 (100.0%) 11 (100.0%) 10 (90.9%)
Consolidation 5 (100.0%) 0 0
Reticulation 5 (100.0%) 9 (81.7%) 10 (90.9%)
Subpleural line 1 (20.0%) 1 (9.1%) 1 (9.1%)
Traction brochiectasis 0 2 (18.2%) 2 (18.2%)
Air trapping 1 (20.0%) 1 (9.1%) 1 (9.1%)
Small nodule 2 (40.0%) 2 (18.2%) 2 (9.1%)
GGO predominance 5 (100.0%) 2 (18.2%)
Reticulation predominance 0 3 (27.3%) 8 (72.7%)
Distribution of peripheral 3 (60.0%) 9 (81.7%) 9 (81.7%)
Distribution on axial section (anterior and
posterior) 5 (100.0%) 11 (100.0%) 10 (90.9%)
Segments involved 48 (48/500) 106 (106/2200) 75 (75/2200)
Table 2. CT findings during follow-up.
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Discussion
During viral lung infections, the lungs histologically show dif-
fuse alveolar damage, including interstitial lymphocyte infil-
tration, air-space hemorrhage, edema, fibrosis, type 2 cell hy-
perplasia, and hyaline tissue formation [19]. Diffuse alveolar
damage is found in some kinds of viral pneumonia, but it is
usually self-limited and radiologic abnormalities usually di-
minish within 3 weeks in immunocompetent patients [20].
In SARS-CoV-infected patients, intralobular and interlobular
septal thickening, subpleural lines, and traction bronchiecta-
sis were observed as late as 84 months after SARS infection
in the present study. All these thin-section CT manifestations
were also found at 3 and 6 months during the recovery phase
A B C
Figure 1. Case 1, SARS survivor, female, 30 years old. (A) The CT scan at 3 months showed diffuse bilateral GGO (arrow). (B) Six
months later, GGO was reduced. (C) At 84 months, GGO was greatly reduced and fine reticulation (intralobular and
interlobular septal thickening) predominated (arrow). Patchy decreased attenuation was seen at 3-, 6-, and 84-month CT
(triangle).
A B C
Figure 2. Case 7, SARS survivor, male, 31 years old. (A) Chest radiography showed consolidation in the lower lobes of both lungs in
acute phase. (B) Six months later, GGO (triangle) and reticulation (arrow) were observed in both lungs. (C) Fine reticulation
(arrow) still persisted but GGO could not be found at 84-month CT.
A B C
Figure 3. Case 6, SARS survivor, female, 32 years old. (A) X-ray radiography showed a large consolidation in the lower lobes of both
lungs in acute phase. (B) Six months later, X-ray revealed GGO, septal thickening, and fine-mesh shadows (white arrow).
Traction bronchiectasis was found in the left lower lobe. (C) At 84 months, GGO was reduced and interlobular thickening
predominated. Traction bronchiectasis was still present.
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of SARS, which may indicate lung fibrosis, as observed in pre-
vious studies [21,22]. To the best of our knowledge, the pres-
ent study is the first to report abnormal imaging at up to 7
years after SARS-CoV pneumonia.
The characteristic thin-section CT finding in SARS survivors
changed from GGO predominance at 3–6 months to fine re-
ticulation (intralobular and interlobular septal thickening)
predominance at 7 years. GGO was found in 8 patients at 6
months and in 2 patients at 84 months. Some studies report-
ed the imaging features of the recovery phase in patients with
SARS [21,22]. Antonio et al. [21] analyzed the thin-section CT
findings at an average of 36.5 days in 24 patients and observed
that the main findings in the recovery phase were GGO, intra-
lobular and interlobular septal thickening, traction bronchi-
ectasis, and subpleural lines. They also reported that fibrosis
began early and tended to be found in elderly and more seri-
ously affected patients. However, in the present study, all 11
patients showed abnormalities that may indicate fibrosis at 6
months, and 10 patients still had signs of lung fibrosis after
7 years. All patients were 30–54 years old when they were in-
fected by SARS-CoV; therefore, lung fibrosis could be a long-
term sequela of SARS-CoV infection.
Importantly, the thin-section CT lung abnormalities observed in
the present study seemed to be different from those induced
by other pneumonia viruses [23,24]. It is known that many
SARS patients suffer from ARDS/DAD in the acute phase [25].
Nevertheless, the present study suggests that either the lung
fibrosis is very slow to disappear after infection or that the CT
abnormality is different from lung fibrosis induced by other
pneumonia viruses. However, the results of the present study
do not resolve this issue. With regard to the physical impair-
ment that may accompany the abnormalities on thin-section
CT, some previous studies suggest that the physical impair-
ment after SARS persists for at least 12 months [11,13], while
another study suggests only mild impairments at 5 years [14].
A study has shown that the immune response after SARS per-
sists for at least 90 days [26], but no data is available to deter-
mine exactly how long it persists and whether it could involve
lungs as a long-term sequela. In our study, mild or moderate
pulmonary function damage was still present in 81.8% of the
patients at 7 years after SARS infection.
Some studies have shown that after the acute phase of ARDS,
CT findings are variable [26–28]. In ARDS, although complete
resolution of abnormalities may occur, the typical CT findings
at the later stage are that of a coarse reticular pattern and GGO
in the anterior part of the lungs [25,27,29]. In this setting, it
is likely that GGO represents areas of fine fibrosis, which are
observed on thin-section CT. Our study shows that the CT ab-
normalities of all patients had a diffuse distribution, which was
similar that reported in a recent study by Masclans et al. [30].
Indeed, Masclans et al. [30] found that 76% of patients had
abnormalities on high-resolution CT at 6 months after infec-
tion, and these abnormalities were typically areas of reticula-
tion and GGO. Therefore, the distribution of thin-section abnor-
malities in our study seem to be different from those reported
in some other studies [25,27,29] on late-stage ARDS. However,
drawing conclusions is impossible because of the lack of ac-
companying histopathological examination in most patients
with SARS and ARDS.
Another finding of the present study is the presence of trac-
tion bronchiectasis, which represents airway abnormalities, as
well as patchy decreased attenuation, which probably repre-
sents airway abnormalities. Traction bronchiectasis was found
in 3 patients, while patchy decreased attenuation was found in
1 patient. Similar results in SARS patients were also reported
in some other studies [24,31]. Masclans et al. [30] found that
airway disease was more common in ARDS survivors, again
suggesting the possibility of the presence of underlying lung
fibrosis in these survivors of SARS.
The present study is not without limitations. This was a retro-
spective review of patients evaluated at 2 centers, with all of
the issues of selection and observational biases that this de-
sign entails. Secondly, the sample size was smaller than that
of prior studies and may not represent most patients. Thirdly,
the pulmonary function test results at 3 and 6 months were
unavailable in most patients.
Conclusions
This study of 11 SARS patients found that lung abnormalities
on thin-section CT still existed in SARS survivors 7 years af-
ter infection, though the extent became less. During convales-
cence after SARS, GGO and intralobular and interlobular sep-
tal thickening were the main thin-section CT manifestations.
From 6 months to 7 years after SARS, the predominant thin-
section CT findings changed from GGO predominance to fine
reticulation predominance, which probably represents the in-
terstitial fibrotic proliferation recovery phase of diffuse alveo-
lar damage. These abnormalities were consistent with the PFT.
Conflict of interest
The authors declare that they have no actual or potential con-
flicts of interest.
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CT during convalescence after SARS
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