AJR 2005; 185:616-621
© American Roentgen Ray Society
Pleuropulmonary Paragonimiasis: CT Findings in 31 Patients
Tae Sung Kim1,
Joungho Han2,
Sung Shine Shim1,
Kyeongman Jeon3,
Won-Jung Koh3,
Inho Lee1,
Kyung Soo Lee1 and
O Jung Kwon3
1 Department of Radiology and Center for Imaging Science, Samsung Medical
Center, Sungkyunkwan University School of Medicine, 50, Ilwon-dong,
Gangnam-gu, Seoul 135-710, Korea.
2 Department of Pathology, Samsung Medical Center, Sungkyunkwan University
School of Medicine, Seoul 135-710, Korea.
3 Division of Pulmonary and Critical Care Medicine, Department of Medicine,
Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul
135-710, Korea.
Received September 25, 2004;
accepted after revision October 28, 2004.
Address correspondence to T. S. Kim.
Supported by grant R11-2002-103 from the Korea Science and Engineering
Foundation.
Abstract
OBJECTIVE. The purpose of our study was to identify any specific CT
features that may help in the diagnosis of pleuropulmonary paragonimiasis.
CONCLUSION. Pleuropulmonary paragonimiasis usually manifests as a
subpleural or subfissural nodule of about 2 cm in diameter that frequently
contains a necrotic low-attenuation area. The constellation of focal pleural
thickening and subpleural linear opacities leading to a necrotic peripheral
pulmonary nodule is another frequent CT finding of paragonimiasis. Although
minimal and easily overlooked, focal fibrotic pleural thickening adjacent to a
pulmonary nodule can be an important clue in the diagnosis of pleuropulmonary
paragonimiasis on CT.
Introduction
Pleuropulmonary paragonimiasis is a food-borne parasitic disease
caused by the lung fluke Paragonimus westermani, which is endemic in
Southeast Asia and the Far East
[1]. Human infection results
from ingestion of raw freshwater crab or crayfish infected with the
metacercaria. According to several articles and case reports on the CT
features of pleuropulmonary paragonimiasis
[2-9],
the common CT findings include pleural effusion, hydropneumothorax, pulmonary
nodules or air-space consolidation, and cysts. We retrospectively reviewed
chest CT images of serologically or histopathologically proven pleuropulmonary
paragonimiasis in 31 patients to identify any other specific imaging
characteristics that may help in the diagnosis of this disease.
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Fig. 1A —45-year-old man with pleuropulmonary paragonimiasis. Axial
contrast-enhanced CT scan (5-mm collimation) at mediastinal window setting
shows 30-mm mass in right upper lobe. Although mass seems to be located
centrally, it is not associated with lobar bronchus but shows subpleural and
subfissural location. Note area of low attenuation (15 H) (arrow) and
enhancing portion (80 H) (arrowhead) of mass.
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Fig. 1B —45-year-old man with pleuropulmonary paragonimiasis. CT scan
at lung window setting shows subpleural and subfissural location of tumor.
Note thickening of minor interlobar fissure (arrows) and mediastinal
pleura (arrowhead).
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Materials and Methods
Between 1995 and September 2004, 31 patients (19 men, 12 women; age range,
19-75 years; mean, 48 years) with serologically (n = 20) or
histopathologically (n = 11) proven paragonimiasis and with chest CT
scans available were identified from the file archives of the department of
pathology and the health medical records department in our institute. Approval
from the institutional review board is not needed for review of medical
records, pathology reports, and radiologic images for research purposes in our
institute. We retrospectively reviewed clinical, CT, and histopathologic
findings of these patients.
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Fig. 1D —45-year-old man with pleuropulmonary paragonimiasis.
Photomicrograph of pathologic specimen from wedge resection shows
granulomatous and fibrous reaction. Intratumoral low-attenuation (15 H) area
on contrast-enhanced CT scan (A) is correlated with multiple granulomas
(arrows) with central necrosis on histopathologic specimen. Enhancing
portion (80 H) of nodule on CT corresponded to organizing pneumonia
(asterisk) with granulation tissue and lymphoid follicles. Note
fibrotic pleural thickening (arrowheads) with some areas of
lymphocytic infiltration. (H and E, x2)
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Fig. 1E —45-year-old man with pleuropulmonary paragonimiasis.
High-power photomicrograph shows multiple eggs (=100 x 50 µm)
(arrowheads) of Paragonimus westermani in wall of granuloma.
Note multiple eosinophils (arrows) in wall of granuloma and central
necrotic portion (asterisk). (H and E, x200)
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Unenhanced thin-section (1- or 1.25-mm collimation at 10-mm intervals) and
contrast-enhanced helical chest CT images (5- or 7-mm collimation
reconstruction) were obtained in 28 patients using helical CT scanners
(HiSpeed Advantage or Light-Speed QX/I, GE Healthcare). In the remaining three
patients, only unenhanced thin-section CT scans were obtained. The parameters
of helical chest CT were 120 kVp, 170 mAs, 5- or 7-mm collimation, and a 10
mm/sec table feed. Contrast-enhanced chest CT scans were obtained after
injection of 30 g of iodinated contrast medium (100 mL of iopamidol [Iopamiron
300, Bracco]) at a rate of 3 mL/sec with a power injector (OP 100, Medrad).
The scan data were displayed directly on monitors (four monitors, 1536 x
2048 image matrices, 8-bit viewable gray-scale, and 60-foot-lambert
luminescence) of a PACS (PathSpeed, GE Healthcare).
Chest CT scans were analyzed retrospectively and jointly by two chest
radiologists with 7 and 2 years of experience in chest radiology,
respectively. Chest CT scans were assessed specifically for the location,
margin, size, and internal characteristics of pulmonary nodules; the presence
or absence of pleural change, adjacent bronchiectasis, and areas of
ground-glass attenuation; and mediastinal or hilar lymphadenopathy. Any other
associated findings were also assessed, including pleural effusion or
pneumothorax. As for the location of pulmonary nodules, central nodules were
defined as those that involved a lobar or segmental bronchus. Peripheral
nodules were defined as those surrounded by lung parenchyma or distal to the
subsegmental bronchi. Subpleural or subfissural nodules were defined as those
abutting the pleura or an interlobar fissure. Mediastinal or hilar lymph nodes
greater than 10 mm in the short axis were regarded as significantly enlarged
nodes. Decisions on the CT findings were reached by consensus.
Pleuropulmonary paragonimiasis was diagnosed by means of enzyme-linked
immunosorbent assay (ELISA) (n = 20), which is an immunoserologic
test for Paragonimus-specific antibodies; sputum cytology (n
= 8); surgical resection (n = 2); and transthoracic needle aspiration
biopsy (n = 1). The confirmative diagnosis was based on positive
results of an ELISA test or the histopathologic detection of eggs of P.
westermani in sputum samples or specimens of surgical excision or
transthoracic needle aspiration biopsy. The time interval between the CT scan
and a confirmative diagnosis was 1-120 days (mean, 20 ± 29 [SD] days).
The CT findings were correlated with histopathologic findings of the resected
pulmonary nodules in two patients by a pathologist with 9 years of experience
and a chest radiologist.
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Fig. 2A —60-year-old man with pleuropulmonary paragonimiasis. Axial
thin-section CT scan (1-mm collimation) at mediastinal window setting shows
5.5-cm mass (asterisk) in right lower lobe. Note 1-cm, poorly defined
subpleural nodule (arrow) in right middle lobe with adjacent
mediastinal pleural thickening (arrowheads).
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Fig. 2B —60-year-old man with pleuropulmonary paragonimiasis. CT scan
at lung window setting shows small subpleural nodule (arrow) with
adjacent bronchiectasis in right middle lobe. Note mass (asterisk) in
right lower lobe, which proved to be squamous cell carcinoma after bilobectomy
of right middle and lower lobes.
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Fig. 2C —60-year-old man with pleuropulmonary paragonimiasis.
Photomicrograph of surgical specimen shows subpleural granuloma
(arrows) in right middle lobe consisting of fibrotic wall and central
necrotic cavity. Note adjacent fibrotic pleural thickening
(arrowheads) and bronchiectasis (asterisks). (H and E,
x2)
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Fig. 2D —60-year-old man with pleuropulmonary paragonimiasis.
High-power photomicrograph shows multiple eggs (arrows) of
Paragonimus westermani lining inner surface of fibrotic wall
(asterisk) of granuloma. (H and E, x200)
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Results
Clinical Findings
The symptoms of the patients before admission included blood-tinged sputum
(55%, 17/31), cough (42%, 13/31), dyspnea (23%, 7/31), chest pain (16%, 5/31),
and fever (16%, 5/31). Two patients (6%) were asymptomatic. The duration of
symptoms, which was available in 24 patients on the review of the medical
records, ranged from 1 week to 26 months (mean, 6.9 ± 7.7 months). A
history of eating pickled freshwater crab (n = 12) or raw freshwater
fish (n = 5) was reported in 17 patients, four patients denied such
an eating history, and the eating history was not available in 10
patients.
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Fig. 3A —43-year-old woman with pleuropulmonary paragonimiasis. Axial
contrast-enhanced CT scan (5-mm collimation) at mediastinal window setting
shows 3-cm subpleural mass in right upper lobe. Note adjacent focal pleural
thickening (arrow).
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The WBC (3.8 x 103/µL < normal range < 10.58
x 103/µL) was increased in nine patients (29% sensitive)
(range, 10.72-14.4 x 103/µL; mean, 12.3 ± 1.2
x 103/µL). The differential count of blood eosinophils (0%
< normal range < 9.3%) was increased in 21 patients (68% sensitive)
(range, 9.5-66%; mean, 19.9% ± 13.5%). The blood eosinophil count
(50/µL < normal range < 500/µL) was increased in 23 patients (74%
sensitive) (range, 548-8,686/µL; mean, 1,747 ± 1,857/µL).
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Fig. 4A —44-year-old man with pleuropulmonary paragonimiasis. CT scan
(5-mm collimation) at lung window setting shows 3-cm, poorly defined
subpleural nodule with pleural effusion in lingular division of left upper
lobe. Note central cavitation and surrounding halo of ground-glass
attenuation.
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CT Findings
The main CT feature of pleuropulmonary paragonimiasis was pulmonary nodules
(Figs. 1A,
1B,
1C,
1D,
1E,
2A,
2B,
2C,
2D,
3A,
3B,
4A,
4B,
5,
6A, and
6B). A single nodule was seen
in 18 patients (58%), two nodules in six patients (19%), and three nodules in
four patients (13%). The remaining three patients all showed more than three
nodules (4, 8, and 15, respectively). In three patients, two or three nodules
were clustered in one pulmonary lobe. The pulmonary nodules were located in
the right upper lobe (n = 12 patients), right middle lobe (n
= 7), right lower lobe (n = 8), left upper lobe upper division
(n = 6), lingular division (n = 7), and left lower lobe
(n = 6). Two patients showed multiple nodules in all pulmonary lobes.
The CT features of pulmonary nodules and other associated CT findings of
pleuropulmonary paragonimiasis and their incidences are summarized in Tables
1 and
2. Subpleural streaky opacity
connecting the pleura and the nodule, which was presumed to be a worm
migration track (burrow track), was 2-7 mm thick and 5-60 mm long.
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Fig. 5 —19-year-old woman with pleuropulmonary paragonimiasis. Axial
thin-section CT scan (1-mm collimation) at lung window setting shows two
cavitary nodules clustered in right upper lobe. Note focal thickening or
indentation of adjacent pleura (arrowhead) and short, subpleural
linear opacity (arrow) connecting pleura and peripheral nodules,
which suggests worm migration track.
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Fig. 6A —42-year-old woman with pleuropulmonary paragonimiasis. Axial
contrast-enhanced CT scan (5-mm collimation) at mediastinal window setting
shows two subpleural masses in right upper lobe, one of which shows cavitation
(arrowhead). Note thickening of adjacent pleura
(arrows).
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Histopathologic Findings and CT-Pathologic Correlation
In nine patients, the sputum cytology or aspiration specimen showed
operculated parasitic eggs of P. westermani. In one patient, a 3-cm
mass was seen in the right upper lobe with a 1-cm hilar lymph node, which was
tentatively diagnosed as lung cancer (American Thoracic Society tumor stage T2
N1) on CT with positive tumor uptake (maximum standardized uptake value, 8.1)
on FDG PET (Figs. 1A,
1B,
1C,
1D, and
1E). Wedge resection of the
tumor was performed, and frozen biopsy revealed granulomatous and fibrous
reaction with eggs of P. westermani. At CT-histopathologic
correlation, the intratumoral low-attenuation (15 H) area seen on
contrast-enhanced CT scans was correlated with necrotic granulomas on the
histopathologic specimen. The enhancing portion (80 H) of the nodule on CT
corresponded to organizing pneumonia with granulation tissue.
In another patient who underwent bilobectomy of the right middle and lower
lobes because of squamous cell carcinoma, another 10-mm subpleural nodule was
found in the right middle lobe (Figs.
2A,
2B,
2C, and
2D). On histopathologic
examination, the subpleural nodule was a granuloma consisting of a fibrotic
wall and a central necrotic cavity in which multiple eggs of P.
westermani were found. In these two cases in which CT-pathologic
correlation was possible, adjacent pleural thickening was composed of fibrotic
thickening with some areas of lymphocytic infiltration.
Discussion
P. westermani is known to migrate in a human host after ingestion
of metacercariae, the infective stage of the parasite. They excyst in the
small intestine, and the larvae penetrate the intestinal wall and enter the
peritoneal space. Next they penetrate the diaphragm and pleura and enter the
lung in 3-8 weeks, where they mature to adult flukes
[1]. According to Im et al.
[3], in a study of radiologic
findings in 71 patients diagnosed with pleuropulmonary paragonimiasis in which
CT scans were available in 17 patients, the characteristic CT features of
paragonimiasis were round low-attenuation cystic lesions (5-15 mm) filled with
either fluid or gas, within the consolidation. On CT, air-space consolidation
was noted in 82% (14/17), nodules in 41% (7/17), linear opacities extending
from the pleura to the lung in 41% (7/17), and bronchiectasis in 35% (6/17).
Subpleural linear opacities or a tubular structure communicating with a cyst
were suggestive of worm migration tracks. On chest radiographs, 83% of
patients had pulmonary lesions (consolidation, cysts, nodule, and linear
opacity) and 61% had pleural lesions (pleural effusion, hydropneumothorax, and
pleural thickening). In their study
[3], pleural thickening was
noted in 7% (5/71) on chest radiography, but its incidence on CT was not
available. In a study of experimentally induced pulmonary paragonimiasis in 21
cats by Im et al. [4], the
appearance of pulmonary lesions varied with the stage of the infection and the
surrounding tissue reaction. Early findings, which were caused by the
migration of juvenile worms, included pneumothorax or hydropneumothorax, focal
air-space consolidation, and linear opacities. Later findings resulting from
worm cysts included thin-walled cysts, masslike consolidation, nodules, or
bronchiectasis. In that experimental study, pleural thickening was noted in
60% (3/5 cats) at 10 or 12 weeks of infection. According to Mukae et al.
[5], in a study of 13 patients
with paragonimiasis, chest radiography and CT showed pleural effusion or
pneumothorax (62%) and parenchymal lesions (92%) with a high frequency of
solitary nodular lesions (62%). According to Matsumoto et al.
[8], CT showed minimal pleural
thickening and adhesions adjacent to the parenchymal lesions in all six
cases.
In our series, the most frequent CT feature of pleuropulmonary
paragonimiasis was a poorly marginated (74%) subpleural or subfissural (87%)
nodule of about 2 cm in diameter that contained a necrotic low-attenuation
area (87%) (Figs. 1A,
1B,
1C,
1D,
1E,
2A,
2B,
2C,
2D,
3A,
3B,
4A, and
4B). The constellation of
focal pleural thickening (87%) and subpleural linear opacities (48%,
presumably worm migration tracks) leading to a necrotic, peripheral, pulmonary
nodule was another typical CT finding of paragonimiasis (Figs.
5 and
6A,
6B). Frequent findings of
adjacent bronchiectasis (55%) and areas of ground-glass attenuation (58%) and
pleural effusion (26%) or spontaneous pneumothorax (10%) can be assessed as
ancillary diagnostic clues for paragonimiasis.
Overall, our results were similar to reported CT findings and the
incidences of pulmonary and pleural lesions
[3,
5]; however, we found a much
higher incidence of focal pleural (87%) or fissural (32%) thickening along
with subpleural streaky opacities (48%) leading to the pulmonary nodules.
Extrapleural fat thickening, which was noted in 29% of cases in our series,
implies a chronic inflammatory process as in empyema
[10]. Although it is minimal
and easily overlooked, focal fibrotic pleural or fissural thickening adjacent
to a pulmonary nodule can be an important clue that the peripheral pulmonary
nodule has originated from the pleural space. Therefore, it can be of help in
the diagnosis of pleuropulmonary paragonimiasis on CT. Although most patients
(87%) in our series showed focal pleural thickening or indentation on CT, four
patients (13%) did not show such a finding. We think these patients were at an
earlier stage of the disease process than other patients because development
of pleural thickening was seen 10-12 weeks after ingestion of metacercariae of
P. westermani in the experimental study using cats
[4]. In one patient whose
follow-up CT scan was available, diffuse thickening of the pleura and the
extrapleural fat, along with a moderate amount of pleural effusion (empyema
appearance), developed 4 months after the initial CT scan in which only a
poorly defined, subpleural cavitary nodule with pleural effusion was noted
(Figs. 4A, and
4B).
According to a case report by Watanabe et al.
[11], pulmonary paragonimiasis
can mimic lung cancer by showing a high FDG uptake on FDG PET. The same
finding was seen in one of our patients, which mandated surgical excision of
the pulmonary nodule.
In our series, among the laboratory data of blood tests, the sensitivities
of blood eosinophil count (74%) and the differential count of blood
eosinophils (68%) were higher than that of the total WBC (29%). Despite
approximately 30% false-negative results, we think the finding of blood
eosinophilia can be helpful in the diagnosis of pleuropulmonary paragonimiasis
because of its relatively high sensitivity.
In conclusion, pleuropulmonary paragonimiasis usually manifests as a poorly
marginated subpleural or subfissural nodule of about 2 cm in diameter that
frequently contains a necrotic low-attenuation area. The constellation of
focal pleural thickening and subpleural linear opacities leading to a necrotic
peripheral pulmonary nodule was another typical CT finding of paragonimiasis.
Other frequent findings include adjacent bronchiectasis, areas of ground-glass
attenuation, and pleural effusion or spontaneous pneumothorax.
Although minimal and easily overlooked, focal fibrotic pleural or fissural
thickening adjacent to a pulmonary nodule can be an important clue in the
diagnosis of pleuropulmonary paragonimiasis on CT.
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Abstract
Introduction
