(Chest. 2001;120:514-520.)
© 2001
American College of Chest Physicians
Clinicoradiologic Features of Pleuropulmonary Paragonimus westermani on Kyusyu Island, Japan*
Hiroshi Mukae, MD;
Haruko Taniguchi, MD;
Nobuhiro Matsumoto, MD;
Hirotoshi Iiboshi, MD;
Jun-ichi Ashitani, MD;
Shigeru Matsukura, MD and
Yukifumi Nawa, MD
*
From the Departments of Internal Medicine III (Drs. Mukae, Taniguchi, Matsumoto, Iiboshi, Ashitani, and Matsukura) and Parasitology (Dr. Nawa), Miyazaki Medical College, Miyazaki, Japan.
Correspondence to: Hiroshi Mukae, MD, The Third Department of Internal Medicine, Miyazaki Medical College, Kiyotake, Miyazaki, Japan 889-1692; e-mail: hmukae{at}post.miyazaki-med.ac.jp
 |
Abstract
|
|---|
Study objective: Recently, the number of new cases of
Paragonimus westermani in humans has gradually increased,
and paragonimiasis is a re-emerging public health issue in Kyusyu,
Japan. We review our recent experience with pleuropulmonary
Paragonimus westermani.
Patients:
Pulmonary paragonimiasis was diagnosed in 13 patients at the Third
Department of Internal Medicine, Miyazaki Medical College between 1993
and 1999.
Results: Both sputum and bronchoscopic
examinations revealed ova in four of nine patients; bronchoscopy
yielded ova in two additional patients. Twelve patients (92%) had
respiratory symptoms, including cough (92%), sputum and/or hemoptysis
(92%), and chest pain (46%). Chest radiography and CT showed pleural
lesions (62%) and parenchymal lesions (92%). Of note was the high
frequency of solitary nodular lesions (62%), mimicking lung cancer,
tuberculosis, or fungal diseases. Immunodiagnosis and bronchoscopic
examination were also useful for diagnosis. Praziquantel treatment was
very effective and had minimal side effects. One patient required
surgical decortication for empyema in spite of treatment with
praziquantel. Eosinophilia was noted in peripheral blood and body
fluids, which was probably due to increased levels of
interleukin-5.
Conclusions: Our findings indicate that
our patients with Paragonimus westermani presented with a
wide variety of radiographic findings, which were different from the
classic presentations reported earlier. Bronchoscopic examination and
serologic tests are very useful for accurate diagnosis. As dietary
habits change and international transportation increases, it appears
likely that paragonimiasis will also increase in frequency in various
parts of the world.
Key Words: clinicoradiologic feature • interleukin-5 • Paragonimus westermani
|
Introduction
|
|---|
Paragonimiasis
is a food-born parasitic disease common in southeast Asia, especially
in Japan, Korea, the Philippines, Taiwan, and parts of
China.1
Furthermore, a highly increasing incidence of
paragonimiasis was observed in eastern Nigeria in from 1967 to
19702
; in the late 1970s, immigration of southeast Asian
refugees resulted in an increased number of reported cases in the
western world.3
4
5
6
In Japan, two species, Paragonimus westermani and
Paragonimus miyazakii, are known as the pathogens of human
paragonimiasis and a majority of paragonimiasis was infection due to
P westermani. Kyusyu Island is the southernmost of the four
major islands of Japan (Fig 1
). Miyazaki prefecture is located in Kyusyu Island (Fig 1)
and has long
been known as one of endemic areas for P. westermani, where > 300
cases were found in the 1950s.7
The inhabitants of
Miyazaki prefecture have a custom of eating freshwater crabs,
Eriocheir japonicus, a famous second intermediate host of
P westermani, or the flesh of wild boars, Sus scrofa
leukomystax, a proven paratenic host.8
After an
extensive survey and treatment by the local government during the 1950s
and 1960s, the number of new reported cases rapidly decreased; by the
late 1970s, paragonimiasis was declared a disease of the past in this
area.7
However, since the late 1980s, the number of new cases of
paragonimiasis has gradually increased in southern
Kyusyu,7
9
10
and 13 cases of pulmonary P
westermani have been diagnosed at the Third Department of Internal
Medicine, Miyazaki Medical College during the last 7 years. Thus,
paragonimiasis is a re-emerging public health issue in Kyusyu, Japan.
We summarize our recent experience of 13 patients with pulmonary
P westermani.
|
Materials and Methods
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All 13 patients with pulmonary P westermani diagnosed
at the Third Department of Internal Medicine, Miyazaki Medical College
between 1992 to 1999 were included in the study. They consisted of 10
men and 3 women (median age, 49 years; range, 25 to 77 years). Six
patients were smokers, and two were ex-smokers. All patients were
confirmed to have P westermani by immunodiagnosis. Briefly,
a multiple-dot enzyme linked immunosorbent assay (ELISA) was used for
routine primary screening of parasite diseases, and binding inhibition
ELISA and/or Ouchterlony’s method were also used for identification of
pathogens (performed in the Department of Parasitology, Miyazaki
Medical College, Miyazaki). Details of the immunodiagnostic methods
have been described previously.9
A full clinical
evaluation was performed in all patients before and repeatedly after
treatment. A systemic review of the chest radiographs and CT scans was
performed in all patients. In some cases, new lesions evolved during
management. These were included in the data analysis. After informed
consent was obtained, thoracocentesis was performed in patients with
pleural effusion to rule out other diseases.11
Bronchoscopy with bronchial brushing and BAL12
were
performed in nine patients. Sputum samples, pleural effusion, and
bronchial samples were stained for cytology and examined for the
presence of eggs. They were also stained with Ziehl-Neelsen and
cultured for acid-fast bacilli. None of these patients had evidence of
malignancy.
In some patients, we measured interleukin (IL)-5 levels in the serum
and/or body fluids using ELISA. Briefly, monoclonal antibody to human
IL-5 (TRFK5; Pharmingen; San Diego, CA) was bound to microtiter plates
by incubation at 4°C overnight. The wells were washed with
phosphate-buffered saline solution containing 0.05% Tween 20.
After blocking with phosphate-buffered saline solution/10% fetal calf
serum for 2 h, samples and recombinant human IL-5 (Pharmingen)
were added to each well and incubated at 4°C overnight. After
washing, secondary antibody (biotinylated antihuman IL-5 monoclonal
antibody) was added to each well and incubated at room temperature for
1 h, followed by an additional 1-h incubation with
peroxidase-conjugated streptavidin. Wells were subsequently washed and
incubated with 0.11 mol/L sodium acetate buffer containing
tetramethylbenzidine for 15 min or until the development of a suitable
color. Reaction was terminated by adding 1.8 mol/L
H2SO4 to each well.
Absorbance was read at 450 nm in an ELISA reader. The detection limit
was 20.0 pg/mL.
|
Results
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Clinical Features
Table 1
summarizes the clinical and laboratory data of each patient. Almost all
patients (92%) reported eating raw foods, especially wild boar meat.
Twelve patients (92%) presented with respiratory symptoms (cough,
n = 12; 92%), sputum and/or hemoptysis (n = 12; 92%), chest pain
(n = 6; 46%), dyspnea (n = 3; 23%), and fever (n = 3; 23%).
Subcutaneous paragonimiasis was seen in one patient (patient 8), and
one patient (patient 5) suffered from repeated bacterial pneumonia in
the right lower lobe for 4 years before hospital admission. Another
patient (patient 13) had been treated for tuberculosis at another
hospital. Calcification was seen in the brain (patient 2) and liver
(patient 6) on CT scan. WBC count was within the normal range in 12
patients (92%), but eosinophilia was detected in peripheral blood of
11 patients (85%). Serum IgE levels were also elevated in 7 of 11
patients (64%).
Chest Radiograph and CT Findings
Patients presented with a variety of radiographic and CT findings
(Table 2 ), probably depending on different stages of migration of the fluke. All
patients had abnormal findings in the lungs that were classified into
three types: pleural lesions, such as pleural effusion and
pneumothorax; intrapulmonary parenchymal lesions, such as nodular and
infiltrative opacity; and a combination of pleural and intrapulmonary
parenchymal lesions (Table 2)
. Pleural effusion was present
unilaterally in nine patients (69%). Of these, two patients also had
pneumothorax on the same side of the lung. One patient (patient 6) had
also transient pericardial effusion (Fig 2
). Intrapulmonary parenchymal lesions were present in 12 patients
(92%). A nodular shadow (2 to 3 cm in diameter) was present in eight
patients (62%), and small nodular lesions (< 1 cm) were seen in four
patients (31%). Cavitation with a nodule was present in two patients
(patients 1 and 7; Fig 3
). Two patients showed a reticular shadow (patient 2 [Fig 4
, bottom] and patient 8). One patient showed an
infiltrate in the right lower lobe because of obstructive pneumonia
(patient 5). Three patients showed atelectasis: compression atelectasis
by massive pleural effusion in two patients (patients 10 and 13) and
atelectasis by stenosis of the orifice of the associated bronchus in
one patient (patient 5). Mediastinal lymphadenopathy was seen in four
patients. Interestingly, radiographic and CT findings changed in four
patients during intermittent examinations before diagnosis. Enlargement
of a nodule was noted in two patients (patients 1 and 2; Fig 4
,
top, middle) within 2 months. In two patients, a
nodule (2 to 3 cm) developed after transient pleural effusion and
pneumothorax (patient 9) or pericardial and pleural effusion (patient
6; Fig 2
).
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Figure 2. Chest CT scan of patient 6 showing pericardial
effusion and mild pericardial thickening, and left pleural effusion.
Six months later, an irregular nodular opacity appeared in the right
upper lung in this patient (Table 2)
.
|
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Figure 3. Chest CT scan of patient 7 showing a well-defined
nodule with cavitation in the right middle lobe. This shadow also makes
contact with the pleura and with satellite lesions and ectatic changes
of draining bronchi.
|
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Figure 4. Chest CT scans of patient 2 showing ill-defined
solitary nodule with spiculation but without pleural indentation in the
right upper-medial lung field (top). Two months later,
enlargement of the nodule with ectatic changes and wall thickening of
associated bronchi were noted (middle). Note the new
development of a 5-cm zone of irregular peripheral consolidation,
including an air bronchogram (bottom).
|
|
Examination of Sputum, Pleural Effusion, and BAL Fluid
As shown in Table 2
, P westermani eggs were detected in
six patients. Ova were found in the sputum of four patients who had a
solitary nodule and in six BAL fluid (BALF) and/or brushing samples
obtained by bronchoscopy from nine patients (Fig 5
). In three of four patients with positive findings for ova in the
sputum, eggs were found in the sputum just 1 day after bronchoscopic
examination (patients 2, 4, and 6). Furthermore, ova were detected in
two patients (patients 1 and 3) only in BALF and/or brushing samples
harvested during bronchoscopy (Table 2)
. Ova were not found in any
pleural effusion samples examined in four patients (Table 2)
.
Bronchoscopic examination showed stenosis of congested and edematous
bronchi in seven patients (78%) with intrapulmonary parenchymal
lesions (Table 2)
. No malignant cells were found by bronchial brushing
and/or biopsy in these lesions. Marked eosinophilia was detected in
body fluids of these patients (Table 2)
.
Treatment
All patients were treated with a high dose (75 mg/kg/d for 2 or 3
days) of praziquantel. One patient with empyema (patient 11) was
additionally treated with bithionol. No serious side effects were
noted, with the exception of mild urticaria in two patients. In
patients with a solitary nodular lesion, treatment resulted in the
resolution of respiratory symptoms and abnormal findings on chest
radiography. Furthermore, IgG antibody titers and peripheral blood
eosinophilia also significantly decreased in these patients within a
few months after treatment with praziquantel. However, associated
bronchiectatic changes were still present after treatment in some
cases. Praziquantel treatment also resulted in resolution of pleural
effusion in all but one patient (patient 11) who required surgical
decortication. However, pleural thickening (n = 3) and/or atelectasis
(n = 2) remained after treatment in some cases.
Serum levels of IL-5
We also measured IL-5 levels in serum samples from 12 patients and
body fluid samples from 7 patients (Table 1)
. Three of 12 patients
showed elevated levels of IL-5 in the serum as compared to levels below
the detection limit found in 8 healthy volunteers. In BALF samples,
IL-5 levels were also elevated in three of four patients. Three of four
patients showed marked elevation of IL-5 levels in pleural effusion.
|
Discussion
|
|---|
We report here the clinicoradiologic features of 13 patients with
pulmonary P westermani. Diagnosis of paragonimiasis can be
established readily in most patients by identifying the typical
operculated ova in the sputum, stools, or pleural
fluid.2
3
4
13
However, in our patients, eggs in the sputum
were found only in four patients (31%); in three of these patients,
eggs were found in their sputum only after bronchoscopic examination.
In addition, no ova were detected in pleural fluid samples. The
diagnosis was, therefore, made serologically by a dot-ELISA method to
detect parasite-specific IgG antibody.9
More than 100 new
cases of paragonimiasis have been diagnosed mainly by this method
between 1986 and 1998 in the Department of Parasitology, Miyazaki
Medical College,9
10
indicating that the dot-ELISA method
for the detection of IgG antibody is very useful for the diagnosis of
paragonimiasis.
To our knowledge, there are no previous studies that have examined the
validity of fiberoptic bronchoscopy for the diagnosis of P
westermani. Our finding that six of nine patients with
intrapulmonary paragonimiasis were found to have ova on cytologic
examination of bronchial brushing and/or BALF indicates that
bronchoscopic examination is also useful for the diagnosis of
intrapulmonary paragonimiasis. Bronchoscopy also showed bronchial
stenosis of bronchi with congested and edematous mucosa in seven of
nine patients. In addition, one patient (patient 5) had repeated
obstructive pneumonia of the right lower lung and atelectasis of the
right middle lobe due to stenosis of segmental bronchi. In some
patients, bronchiectatic changes were also seen (Fig 3
, 4
,
middle). In this regard, previous reports also indicated
that cystic changes were the main manifestations of paragonimiasis on
chest radiography.2
13
14
Taken together, P
westermani seems to cause marked damage to the bronchi.
To our knowledge, there are few comprehensive reports of the CT
findings in pulmonary P westermani.14
In our
series, patients exhibited a variety of radiographic and CT findings.
Of interest was the high frequency of pleural lesions (69%). A
comprehensive report of the radiographic changes in pulmonary
paragonimiasis by Ogakwu and Nwokolo,2
who studied 100
cases in eastern Nigeria, did not emphasize the presence of pleural
lesions. However, consistent with our data, other
reports3
6
14
described the presence of pleural effusion
as one of the clinical manifestation of P westermani. One
possible explanation for this difference in the incidence of pleural
lesions is that patients reported by Ogakwu and Nwokolo2
included only ova-positive patients, whereas our data emphasize the
diagnostic importance of serologic tests. Our results indicate that
pleural lesions are a common manifestation of P westermani.
With respect to intrapulmonary lesions in paragonimiasis, four patterns
were described by Ogakwu and Nwokolo2
; the most common
shadows were well-defined patches of cavitation, ill-defined "cotton
wool" lesions, "streaky" shadows, or "bubble" cavities. These
patterns were predominantly in the mid-zones of the lungs. A somewhat
different radiographic presentation was, however, observed by Johnson
and Johnson,6
which included diffuse (44%) and segmental
(24%) infiltrates, nodules (20%), and cavities (20%). Ring shadow
was the most prominent lesion in a study of 38 cases in
Thailand,13
and airspace consolidation (45%) and cyst(s)
(46%) were most common in Korea.14
Interestingly, in our
series, the most common lesion was a nodular shadow (62%), a pattern
different from the above-mentioned studies. Chest CT scans revealed
that each nodule was subpleural and occasionally accompanied by ectatic
changes in associated bronchi. Differential diagnosis of pulmonary
paragonimiasis should, therefore, include lung cancer, tuberculosis,
and fungal infection.
A typical route of migration of P westermani in human or
other natural final host is as follows: when metacercariae, the
infective stage of the parasite, are ingested by the final host, they
excyst in the intestine and penetrate the abdominal cavity. The larvae
migrate through the peritoneum, liver, diaphragm, and pleura into the
lung, where they mature to adult flukes.1
Two patients
presented here showed a typical clinical feature of paragonimiasis with
transient pleural effusion and pneumothorax (patient 9) or pericardial
and pleural effusion (patient 6) followed by a nodular shadow in the
lung about 6 months later, which was consistent with the migratory
route of Paragonimus worms. Because of the complexity of the migration
route in the final host, this parasite often causes an ectopic
infestation at various sites, such as the skin, liver, kidney,
peritoneum, spinal cord, or brain.1
In this study,
subcutaneous paragonimiasis was seen in one patient (patient 8). In
addition, calcified lesions were found in the liver (patient 6) and
brain (patient 2), which might be manifestations of extrapulmonary
paragonimiasis.
Studies evaluating the usefulness of bithionol for paragonimiasis, a
drug initially developed as an antihelminthic for veterinary use,
confirmed its effectiveness against paragonimiasis.1
Unfortunately, however, the pharmaceutical company has recently stopped
production of this drug. The alternative agent, praziquantel, has
proven to be effective for paragonimiasis.15
16
Headache,
nausea, and urticaria have been reported as adverse effects during its
use.15
Our study confirmed that praziquantel treatment, 75
mg/kg/d for 2 to 3 days, was very useful and safe. However, ectatic
changes in associated bronchi, pleural thickening, or passive
atelectasis were still present after treatment in some patients. In
addition, one patient in our study required decortication for chronic
empyema. This was consistent with a previous report17
documenting the need for a similar surgery for chronic empyema in 16 of
58 patients infested with P westermani. Thus, early
diagnosis and treatment with praziquantel is necessary for
paragonimiasis.
IL-5, a potent eosinophil chemotactic and growth
factor,18
19
seems to play a major role in
parasite-induced eosinophilia. However, there are only few
studies20
21
22
that have examined the relationship between
IL-5 and paragonimiasis. In this study, eosinophilia was noted in the
serum and/or other body fluids. In addition, high levels of IL-5 also
were detected in the serum and/or other body fluids, particularly in
pleural effusion in some patients. These findings suggest that IL-5 may
play an important role in the pathogenesis of eosinophilic infiltration
in the lung of patients with paragonimiasis.
In conclusion, our patients with P westermani presented with
a wide variety of radiographic findings of intrapulmonary and pleural
lesions, which were different from the classic presentations reported
earlier by other investigators.2,6,13,14 Our results
also indicated that bronchoscopic examination and serologic tests are
very useful for accurate diagnosis. Eosinophilia noted in the serum and
body fluids could be relevant to IL-5 in paragonimiasis. Although
paragonimiasis is rarely seen in Europe and North America, our
speculation is that it will be encountered in the future more
frequently in various parts of the world due to changing dietary habits
and increasing international transportation.
|
Footnotes
|
|---|
Abbreviations: BALF = BAL fluid;
ELISA = enzyme-linked immunosorbent assay; IL = interleukin
Received for publication May 31, 2000.
Accepted for publication January 3, 2001.
|
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Mukae, H, Kadota, J, Kohno, S, et al (1995) Increase in activated CD8+ cells in bronchoalveolar lavage fluid in patients with diffuse panbronchiolitis. Am J Respir Crit Care Med 152,613-618[Abstract]
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Suwanik, R, Harinsuta, C (1959) Pulmonary paragonimiasis: an evaluation of roentgen findings in 38 positive sputum patients in an endemic area in Thailand. AJR Am J Roentgenol 81,236-244
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Im, J-G, Whang, HY, Kim, WS, et al (1992) Pleuropulmonary paragonimiasis: radiologic findings in 71 patients. AJR Am J Roentgenol 159,39-43[Abstract/Free Full Text]
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Johnson, RJ, Jong, EC, Dunning, SB, et al (1985) Paragonimiasis: diagnosis and the use of praziquantel in treatment. Rev Infect Dis 7,200-206[ISI][Medline]
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Monson, MH, Koenig, JW, Sachs, R (1983) Successful treatment with praziquantel of six patients infected with the African lung fluke, Paragonimus uterobilateralis. Am J Trop Med Hyg 32,371-375
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Dietrick, RB, Sade, RM, Pak, JR (1981) Results of decortication in chronic empyema with special reference to paragonimiasis. Thorac Cardiovasc Surg 82,58-62
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Clutterbuck, EJ, Sanderson, CJ (1990) Regulation of human eosinophil precursor production by cytokines: a comparison of recombinant human interleukin-1 (rhIL-1), rhIL-3, rhIL-5, rhIL-6, and rh-granulocyte-macrophage colony-stimulating factor. Blood 75,1774-1779[Abstract/Free Full Text]
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TOP
Abstract
Introduction
