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
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.
(CHEST 2001; 120:514 –520)
Key words: clinicoradiologic feature; interleukin-5; Paragonimus westermani
Abbreviations: BALF ⫽ BAL fluid; ELISA ⫽ enzyme-linked immunosorbent assay; IL ⫽ interleukin
aragonimiasis is a food-born parasitic disease
P 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– 6
In Japan, two species, Paragonimus westermani
and Paragonimus miyazakii, are known as the patho*From the Departments of Internal Medicine III (Drs. Mukae,
Taniguchi, Matsumoto, Iiboshi, Ashitani, and Matsukura) and
Parasitology (Dr. Nawa), Miyazaki Medical College, Miyazaki,
Japan.
Manuscript received May 31, 2000; revision accepted January 3,
2001.
Correspondence to: Hiroshi Mukae, MD, The Third Department of
Internal Medicine, Miyazaki Medical College, Kiyotake, Miyazaki,
Japan 889-1692; e-mail: [email protected]
gens 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
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Clinical Investigations
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 phosphatebuffered 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
Clinical Features
Figure 1. Map of Japan.
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
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)
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
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515
Table 1—Clinical and Laboratory Data*
Patient
Age, yr
Sex
Eating Custom
Symptoms
1
41
M
Unknown
2
3
4
5
64
77
25
37
F
M
M
M
Freshwater crabs
Flesh of wild boars
Flesh of wild boars
Flesh of wild boars
6
61
F
Freshwater crabs
7
49
M
Flesh of wild boars
Cough, hemoptysis, chest
pain, fever
Cough, hemoptysis
Cough, hemoptysis
Asymptomatic
Cough, sputum, fever,
repeated pneumonia
(right lower)
Chest pain, cough36
mo3cough,
hemoptysis
Cough, hemoptysis
8
69
F
Freshwater crabs
Cough, sputum
9
66
M
Flesh of wild boars
10
11
43
57
M
M
12
41
M
Flesh of wild boars
Flesh of wild boars,
freshwater crabs
Freshwater crabs
13
44
M
Flesh of wild boars
Cough, chest pain36
mo3cough,
hemoptysis
Cough, sputum
Cough, hemoptysis, chest
pain, dyspnea, fever
Cough, dyspnea, sputum,
chest pain
Cough, exertional
dyspnea, chest pain,
sputum
Eosinophils in
Body Fluid,
%
Leukocytes, No.
(% Eosinophil)
IgE, IU/mL
8,700 (4.7)
ND
⬍ 20 (serum)
5,400 (7.4§)
6,400 (17.7§)
7,200 (7.4§)
5,800 (8.0§)
2,338.8‡
3,120.7‡
125.9
27,378.1‡
69 (BALF)
29 (serum)
⬍ 20 (serum)
⬍ 20 (serum)
32.3 (serum)
5,400 (9.8§)
1,832.9‡
87 (BALF)
⬍ 20 (serum)
⬍ 20 (BALF)
866.0‡
34 (BALF)
ND
95 (PF)
90 (BALF)
⬍ 20 (serum)
440 (BALF)
⬍ 20 (serum)
29,800 (PF)
55.8 (BALF)
⬍ 20 (serum)
37.4 (BALF)
6,200 (12.0§)
10,900† (45.0§)
5,800 (22.8§)
31.8
15 (BALF)
7,100 (8.6§)
7,200 (0.4)
659.6‡
192.1
2 (PF)
6,800 (17.4§)
365.0
87 (PF)
8,000 (38.6§)
2,918.9‡
94 (PF)
IL-5, pg/mL
ND
⬍ 20 (serum)
⬍ 20 (PF)
⬍ 20 (serum)
3696 (PF)
38.8 (serum)
2100 (PF)
*ND ⫽ not done; PF ⫽ pleural fluid.
†Normal range ⫽ 5,000 to 9,000.
‡Normal range ⫽ ⬍ 394 IU/mL.
§Normal range ⫽ 0.7 to 7.0.
(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).
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).
Examination of Sputum, Pleural Effusion, and BAL
Fluid
Treatment
As shown in Table 2, P westermani eggs were
detected in six patients. Ova were found in the
All patients were treated with a high dose (75
mg/kg/d for 2 or 3 days) of praziquantel. One patient
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Clinical Investigations
Table 2—Chest Radiographic and Bronchoscopic Findings*
Ova
Patient
Radiographic and CT Findings
1
3
Nodule (left upper, 2.5 cm, transient cavity),
mediastinal lymphadenopathy, pleural thickness32
mo3enlargement of nodule
Nodule (right upper, 3 cm), small nodule (right
middle, 0.3 cm), mediastinal lymphoadenopathy32
mo3plus infiltrate (right upper), enlargement of
nodule (right upper)
Nodule (left lower, 2 cm), transient PE
4
Nodule (right upper, 3 cm)
5
Nodule (right lower, 3 cm), atelectasis (right middle),
infiltrate (right lower)
Pericardial effusion, PE (left)36 mo3nodule (right
upper, 3 cm)
2
6
7
8
9
10
11
12
13
Nodule (right middle, 3 cm), mediastinal
lymphadenopathy
Reticulonodular (right upper); PE (left)
PE, pneumothorax (left), small nodules (right, ⬍ 1
cm)36 mo3nodule (right upper, 3 cm),
mediastinal lymphadenopathy
Right PE, compression atelectasis (right lower)
PE (right)
PE, pneumothorax (right), small nodules (right ⬍ 1
cm), mediastinal lymphadenopathy
PE, compression ateletasis (right), small nodule (right
upper, ⬍ 1 cm)
Sputum
BF
PE
Normal finding
⫺
Brushing ⫹,
washing ⫹
ND
Stenoses of right B1 and B2 with
edematous and reddish musosa
⫹
Brushing ⫹,
BALF ⫹
ND
Stenosis of left B6 with
edematous and reddish musosa
Stenosis of right upper bronchus
with edematous and reddish
musosa
Stenoses of right B5a and B6
with edematous and reddish
Stenosis of right upper bronchus
with edematous and reddish
mucosa
Stenosis of right B4 with
edematous and reddish
Normal finding
⫺
Brushing ⫹
ND
⫹
Brushing ⫹
ND
⫺
Brushing ⫺,
BALF ⫺
Brushing ⫹,
BALF ⫹
ND
Brushing ⫺,
BALF ⫹
Brushing ⫺,
BALF ⫺
Brushing ⫺,
BALF ⫺
ND
Bronchoscopic Findings
⫹
⫹
⫺
⫺
ND
⫺
Stenosis of right B2 with
edematous and reddish
mucosa
ND
ND
ND
ND
⫺
⫺
⫺
ND
ND
ND
ND
⫺
⫺
ND
⫺
ND
⫺
*PE ⫽ pleural effusion; ⫹ ⫽ positive; ⫺ ⫽ negative; BF ⫽ bronchofiberscope; see Table 1 for expansion of other abbreviation.
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
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).
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 5. A Paragonimus ovum in the BALF of patient 7
(Papanicolaou stain, original ⫻ 400).
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
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).
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.
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– 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 bron-
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choscopy 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 midzones 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 parasiteinduced eosinophilia. However, there are only few
studies20 –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 imporCHEST / 120 / 2 / AUGUST, 2001
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519
tant 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.
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Clinical Investigations