Parasitology International 64 (2015) 274–280

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Case Report

A rare case of paragonimiasis miyazakii with lung involvement diagnosed 7 years after infection: A case report and literature review Kazuhiro Yatera a,⁎, Minako Hanaka a, Tetsuya Hanaka a, Kei Yamasaki a, Chinatsu Nishida a, Toshinori Kawanami a, Yukiko Kawanami a, Hiroshi Ishimoto a, Tamotsu Kanazawa b, Hiroshi Mukae a a b

Department of Respiratory Medicine, University of Occupational and Environmental Health, Japan, 1-1, Iseigaoka, Yahatanishiku, Kitakyushu City, Fukuoka 807-8555, Japan Department of Immunology and Parasitology, University of Occupational and Environmental Health, Japan, 1-1, Iseigaoka, Yahatanishiku, Kitakyushu City, Fukuoka 807-8555, Japan

a r t i c l e

i n f o

Article history: Received 10 December 2014 Received in revised form 7 February 2015 Accepted 16 February 2015 Available online 11 March 2015 Keywords: Paragonimus miyazakii Paragonimus skrjabini Eosinophilic pneumonia Corticosteroid Bronchoalveolar lavage fluid Paragonimiasis

a b s t r a c t We report a rare case of pulmonary paragonimiasis caused by Paragonimus miyazakii that showed pulmonary manifestations and a long-term clinical course after infection. A 45-year-old Japanese male developed cough and dyspnea in 2004 and was diagnosed with eosinophilic pneumonia. He had been treated with low-dose oral corticosteroid for 7 years. He recalled that he had consumed a large amount of raw freshwater crab (Geothelphusa dehaani) several weeks before he had been admitted for the first time, and that had been the only occasion when he had eaten this meat. The patient was referred to our hospital due to persistent hemoptysis, and his chest computed tomography scan showed pulmonary nodules and cavities, and his serum total IgE level was elevated. Bronchoscopy was performed, and ova were detected in the bronchoalveolar lavage fluid. The morphological examination of the ova and immunoserological examination yielded typical findings of P. miyazakii. Treatment with praziquantel improved his chest radiographic findings and a decrease of serum total IgE, as well as the values of immunoserological examination for P. miyazakii. The clinical course of this patient indicated that he had been infected with P. miyazakii for 7 years at least, which is unusual for paragonimiasis miyazakii. © 2015 Elsevier Ireland Ltd. All rights reserved.

1. Introduction

2. Case report

Paragonimiasis is a food-borne parasitic disease, and there are two species, Paragonimus westermani and Paragonimus miyazakii, that infect human in Japan. The prevalence of this disease drastically decreased because of an improvement of hygiene. Pulmonary manifestations such as nodules, consolidations, and cysts are typical features of paragonimiasis westermani, but not of paragonimiasis miyazakii, because human is a suitable host for P. westermani and an unsuitable host for P. miyazakii. We herein report a rare case of pulmonary P. miyazakii infection that showed a very long clinical course of pulmonary manifestations for 7 years after infection.

A 45-year-old Japanese male presented with a nonproductive cough in November 2004. He was a smoker and chance alcohol drinker and had no remarkable family or past medical histories. He had consumed a large amount quantity of raw freshwater crab (Geothelphusa dehaani) for fun with business partners in the summer of 2004 in the mountains in Mie prefecture in Japan, but he had no history of eating wild boar meat. Several weeks later, he was admitted to hospital “A” because of right pneumothorax and bilateral pulmonary infiltrations. A bronchofiberscopic examination revealed massive eosinophils in the bronchoalveolar lavage fluid with peripheral blood eosinophilia, and based on these observations, a diagnosis of eosinophilic pneumonia was made. He was treated with right chest tube drainage and an oral corticosteroid (0.5 mg/kg body weight of prednisolone). The pulmonary infiltration improved after the treatment. He was transferred to hospital “B” with a tapering of the prednisolone. His pulmonary infiltration had been controlled with a maintenance dose of 5 mg of prednisolone from November of 2009 (Fig. 1A), but the pulmonary nodules had continued to persist, although in new locations (Fig. 1B). After transferring to hospital “C” due to a job transfer in April of 2011, he started to have bloody sputum. Chest radiographs (Fig. 1C)

⁎ Corresponding author at: Department of Respiratory Medicine, University of Occupational and Environmental Health, Japan, 1-1, Iseigaoka, Yahatanishiku, Kitakyushu, Fukuoka 807-8555, Japan. Tel.: + 81 93 691 7453; fax: + 81 93 602 9373. E-mail address: [email protected] (K. Yatera).

http://dx.doi.org/10.1016/j.parint.2015.02.009 1383-5769/© 2015 Elsevier Ireland Ltd. All rights reserved.

K. Yatera et al. / Parasitology International 64 (2015) 274–280

A

B

D

E

F

G

H

275

C

Fig. 1. The chest radiography and computed tomography findings of the patient. Chest radiographs taken in 2009 (A), 2010 (B), and September 2011 (C), showed multiple wandering nodules in bilateral lung fields. (D) Grocott staining of the ova in the bronchoalveolar lavage fluid. The average size of the ova was 74.8 × 46.5 μm, the shape was symmetrical, and the thickness of the opposite side of the operculum was thin, suggestive of Paragonimus miyazakii, although the operculum was detached by the preparation of bronchoalveolar lavage sample. Chest computed tomography (CT) was performed at the first visit to our hospital in September 2011 (E, G) and after the treatment in November 2011 (F, H). Several round nodules, funicular shadows and cavities in the right upper and left lower lobes were improved after treatment with praziquantel.

and computed tomography (CT) (Fig. 1E, F) revealed cystic lesions with small nodular opacities in the right upper and left lower lobes, and he was referred to our university hospital in September 2011 to treat these findings. He was afebrile and exhibited normal blood pressure, pulse rate, and SpO2. No abnormal physical findings were observed at his first visit to our hospital. The laboratory findings (Table 1) were within the normal limits, including the eosinophils, except for a high level of IgE-radioimmunosorbent test (1,362 U/ml). Chest radiography (Fig. 1C) and chest high-resolution computed tomography (Fig. 1E, F) showed pulmonary round nodules, funicular opacities and cavitary lesions in the right upper and left lower lobes. Fiberoptic bronchoscopy was performed, and bronchoalveolar lavage fluid (BALF) was recovered from the left S10. Nine symmetrical parasitic ova were observed in the BALF, and the average size of the ova was 74.8 × 46.5 μm, and the thickness of the opposite side of the operculum was thin (Fig. 1D). These typical features of the ova and the operculum were morphologically suggestive of P. miyazakii infection rather than P. westermani. In addition, IgG multiple-dot enzyme-linked immunosorbent assay (ELISA) was solely positive for P. miyazakii and patient's serum diluted at 1 to 900 showed stronger binding to P. miyazakii antigen than to P. westermani antigen in microtiterplate IgG-ELISA (optical densities at 405 nm, Fig. 2) [1,2], also suggestive of P. miyazakii infection. After treatment with praziquantel (75 mg/kg/day for 3 days), his respiratory symptoms and pulmonary shadows showed improvements (Fig. 1G, H), serum levels of total IgE decreased (from 1,362 to 762 U/ml), and optical densities at 405 nm in microtiterplate IgG-ELISA for P. miyazakii also decreased (Fig. 2). Table 2 shows the previously reported cases of P. miyazakii infection with pulmonary involvement. So far, a total of 46 cases including this case have been reported in the literature since 1974, mainly in Japan. Average age and age distribution was 39.0 and from 22 to 77 years old, respectively, and female/male ratio was 31/13 (two cases were

unknown). Ova were detected only in three (6.5%) patients ,including the present case, and all of these three cases had received corticosteroids. Thirty-five (76.1%) cases had a previous history of eating Geothelphusa (Potamon) dehaani or brawn, and the pulmonary involvement of P. miyazakii was first observed between 4 weeks and several years after the consumption of these animals. Eleven (23.9%) of these 46 cases were reported to have received oral corticosteroids before the diagnosis of pulmonary involvement of P. miyazakii, and intrapulmonary findings were observed between 4 weeks and 7 months

Table 1 The laboratory findings at the initial visit. Hematology

Biochemistry

Serology

WBC 5,300/ml Neu 75.6% Lym 17.7% Mon 4.0% Eos 2.01% Bas 0.6% RBC 477 × 104/ml Hb 15.0g/dl MCV 92.7 fl MCH 31.4 ph = g MCHC 33.9 % Plt 23.7 × 104/ml

TP 7.9 g/dl Alb 4.4 g/dl T-bil 07. mg/dl AST 29 IU/l ALT 36 IU/l LDH 185 IU/l BUN 14 mg/dl Cre 0.98 mg/dl Na 140 mEq/dl K 4.8 mEq/l Cl 102 mEq/l Glu 98 mg/dl

CRP 0.08 mg/dl lgG 1986 mg/dl lgA 291 mg/dl lgM 99 mg/dl lgE RIST 1362 U/ml Aspergilus Ag 0.1 C 1 Cryptococcus Ag (−) PR-3 ANCA b10 MPO-ANCA b10 β-D glucan b6.0 pg/ml

Abbreviations: WBC = white blood cell count, Neu = neutrophils, Lym = lymphocytes, Eos = eosinophils, Baso = basophils, Mono = monocytes, RBC = red blood cells, Hb = hemoglobin, Ht = hematocrit, Plt = platelets, TP = total protein, Alb = albumin, T-Bil = total bilirubin, AST = aspartate aminotransferase, ALT = alanine aminotransferase, LDH = lactate dehydrogenase, γ-GTP = gamma-glutamyl transpeptidase, ALP = alkaline phosphatase, BUN = blood urea nitrogen, Cre = creatinine, Glu = glucose, CRP = C reactive protein

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K. Yatera et al. / Parasitology International 64 (2015) 274–280

Fig. 2. The changes of optical densities at 405 nm in microtiterplate IgG-ELISA of the patient's serum for paragonimiasis before and after praziquantel treatment. The optical densities at 405 nm of IgG-enzyme-linked immunosorbent assay (ELISA) of the patient's serum against both Paragonimus miyazakii and P. westermani were measured by a microtiterplate IgG-ELISA. Each bar represents the result of single measurement. The patient's serum diluted at 1 to 900 and 1 to 2700 showed stronger binding to P. miyazakii antigen than to P. westermani antigen, and these optical densities reduced over time after the treatment with praziquantel.

after starting to receive the oral corticosteroid treatment, except for the present case. 3. Discussion This present patient showed two unusual and interesting clinical findings for paragonimiasis caused by P. miyazakii. First, ova of P. miyazakii were detected in the bronchoalveolar lavage fluid. Second, the pulmonary lesions of this patient had been active for over 7 years after the infection with P. miyazakii. Paragonimiasis is a subacute or chronic inflammatory disease caused by eating raw, undercooked, or pickled freshwater crustaceans that contain infective parasite forms (metacercariae) [3]. Although the prevalence of paragonimiasis drastically decreased in the 1970s due to the nationwide survey, treatment, and prevention campaigns in Japan, recently, new patients including immigrants from endemic countries have been re-emerging from the late 1980s. Recent report of Nagayasu et al. [4] demonstrated that a quarter of the cases were immigrants (mostly from China, Thailand, and Korea), whereas the majority of the domestic cases were residents of Kyushu island. Among the more than 40 species of known genus Paragonimus, P. westermani and P. miyazakii are the most important trematodes in Japan. P. miyazakii is a primary member of the Paragonimus skrjabini species complex and is most commonly referred to as the subspecies P. skrjabini miyazakii. After oral infection, the metacercariae of P. westermani enter the peritoneal cavity through the intestinal wall, migrate into the abdominal wall and diaphragm, and finally the reach pleural cavity and the lung, where they mature into the adult form of worms and produce their eggs [5]. This migration process usually takes several weeks. They commence laying eggs in the lungs and can live there for several years [6]. Parenchymal lesions in the lungs, such as pulmonary nodules, consolidation, and cystic lesions, are known to be typical features of paragonimiasis westermani. On the other hand, whereas pleural lesions, such as pneumothorax and pleural effusions are often seen in patients with paragonimiasis caused by P. miyazakii because humans are unsuitable hosts for P. miyazakii [7]. Juvenile worms of P. miyazakii usually cannot mature into adult worms in humans [8]. However, juvenile worms of P. miyazakii migrate to the pleural

cavity; therefore, pleural manifestations are main clinical features of patients infected with P. miyazakii, and the ova of P. miyazakii are not detected in sputum, bronchoalveolar wash, or stool samples. However, parasite eggs were detected in the bronchial lavage fluid in the present patient. The present patient had been treated with an oral corticosteroid for a presumed diagnosis of eosinophilic pneumonia for 7 years at least. The corticosteroid therapy was probably effective in terms of decreasing the pulmonary infiltrations, nodules, and consolidations of this patient, but unfortunately, the radiological information from A hospital where the patient was first treated was no longer available when he visited our hospital. The chest radiological findings of this patient showed exacerbations and remissions between 2009 and 2010, demonstrating wandering of “worm tract” that may be suggestive of P. miyazakii developed into adult worms. In addition, this patient did not show peripheral blood eosinophilia at the first visit to our hospital. Eosinophilia is a major clue to the correct diagnosis of paragonimiasis, and more than 80% of paragonimiasis patients show peripheral blood eosinophilia and/or an elevation of serum total IgE [3]. Moreover, patients with parenchymal lesions had been reported to show relatively lower peripheral eosinophil counts than patients with pleurisy [3,9], indicating that eosinophilia is rather an acute phase response of the host. Long clinical course of the present patient might explain the absence of peripheral eosinophilia, and the long-term treatment with the oral corticosteroid may also have led to these rare clinical findings and the unusual clinical course of this patient. Some patients especially with pulmonary parenchymal lesions have normal peripheral blood eosinophil counts; therefore, a lack of eosinophilia does not necessarily rule out the possibility of paragonimiasis. Several previous reports have shown that eggs and worm cysts of P. miyazakii were formed in the lungs of humans, and some reports also indicated that the patients had taken steroid therapy, similar to the present patient [10–12]. The effects of corticosteroid treatment on the migration and life cycle of P. miyazakii are not well understood at present, but the effect of corticosteroid treatment on the growth of P. miyazakii was first reported by Hashiguchi and Hirai in rat model [13]. Imai et al. [11] and Yamamoto et al. [12] reported that corticosteroids may help P. miyazakii to become mature adult worms and form worm cysts. However, Kojima et al. [14] reported that eggs and worm cysts of P. miyazakii were formed in the lungs of humans without steroid therapy and suggested that P. miyazakii can mature into adult worms in the human body when there is a high level of infection, or that P. miyazakii may be able to have a similar life cycle to P. westermani under certain environments, such as that induced by corticosteroid treatment. A review of the 46 previously reported cases of P. miyazakii with pulmonary involvement including the preset case (Table 2) demonstrated that 35 (76.1%) cases had a previous history of eating suspect organisms, mostly Geothelphusa (Potamon) dehaani, and eleven (23.9%) of these 46 cases had received oral corticosteroids before showing the pulmonary involvement between 4 weeks and 7 months after starting to receive the oral corticosteroid except for this patient. This relatively high percentage of patients receiving oral corticosteroids among the P. miyazakii patients with pulmonary involvement in this review may suggest that corticosteroid treatment may have a precipitative effect on the development of intrapulmonary involvement in patients with P. miyazakii infection. In addition, only three cases who had been treated with an oral corticosteroid showed a recovery of the eggs of P. miyazakii from respiratory samples (sputum and BALF), so it may be relatively difficult to confirm the presence of P. miyazakii eggs in patients with pulmonary involvement. In contrast, the BALF may be useful to detect the eggs of P. miyazakii in patients receiving corticosteroid treatment, as it was in our patient. Since chest radiological findings of paragonimiasis are nonspecific, and differential diagnoses such as bacterial pneumonia, eosinophilic pneumonia, lung cancer, organizing

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Table 2 Reported cases of P. miyazakii with the intrapulmonary involvement. Case no.

Age

Sex

Nationality

Initial symptoms

Eating history of raw meet before first symptom

Eating history before pulmonary involvement

Raw food eaten

1 2 3 4

44 26 53 45

M F M F

Japanese Taiwanese Japanese Japanese

4M 2M 18 M 3M

7M 2M 18 M 9M

P. P. P. P.

5

36

F

Thai

Rt. chest pain and dyspnea Cough, fever, lt. chest pain Cough, fever Productive cough, rt. chest pain, general fatigue Lt. chest pain

Unknown

P. dehaani

6

46

M

Japanese

Back pain

Unknown (childhood) large amount 9M

9M

P. dehaani

7 8 9

47 77 58

M F M

Japanese Japanese Japanese

None Hemosputa, body weight loss Hemosputa, rt. chest pain

2–3 Y 5M Several Y

2–3 Y 7M Several Y

P. dehaani P. dehaani Brawn

10 11 12 13

44 47 27 24

M M M M

Japanese Japanese Japanese Japanese

Rt. chest pain, dyspnea Chest pain Eyelid swelling Bilateral chest pain, back pain

1M 2M 19 M 14 M

1M 23 M 19 M 14 M

P. P. P. P.

14 15

24 22

F M

Japanese Japanese

Bilateral back pain, hemosputa, dyspnea Sputum production

2W 5W

4W 6W

P. dehaani P. dehaani

16 17 18 19

24 24 46 41

M M M M

Japanese Japanese Japanese Japanese

Lt. back pain, productive couhg Low grade fever, lt. chest and back pain None Abdomoinal pain

2M 16 M Several M 4M

2M 21 M Several M 11 M

P. P. P. P.

20 21 22 23

– 52 42 25

– F M M

Unknown Japanese Japanese Japanese

N/A 6Y 3M Unknown

N/A 8Y 4M 3M

N/A P. dehaani P. dehaani P. dehaani

24

47

M

Japanese

Several M

Several M

P. dehaani

25

28

M

Japanese

N/A Convulsion Rt. chest pain Asymptomatic (eosinophilia, abnormal findings on electrocardiogram) Chest pain, recurrent episodes of heart failure Urticarial rash, general itching

2Y

2Y

P. dehaani

26 27 28 29 30 31 32 33

37 25 56 23 31 – 34 42

M M M M M – F M

Japanese Japanese Japanese Japanese Japanese Unknown Japanese Japanese

Dry cough Convulsion Cough Speech disability, weakness Fever up, chest pain N/A Productive cough, fever up, dyspnea Cough, chest pain

N/A 18 M 3M N/A N/A N/A 2M Unknown

N/A 18 M 3M N/A N/A N/A 3M 1M

P. dehaani P. dehaani P. dehaani N/A N/A N/A P. dehaani Unknown

34 35 36 37 38

51 44 42 29 26

F M M F M

Japanese Japanese Japanese Thai Japanese

N/A N/A N/A N/A 2M

N/A N/A N/A 2Y 3M

N/A N/A P. dehaani P. dehaani P. dehaani

39 40 41 42 43 44 45

44 30 28 25 62 44 51

F M M M F F F

Japanese Japanese Japanese Japanese Japanese Japanese Japanese

(chest X-ray abnormality) Hemosputum Lt. hypochondrial pain, general fatigue Transient lt. upper limb paralysis Rt. chest pain, headache, vomiting, transient lt. hemiplegia, hemosputum Cough Chest pain, fatigue N/A N/A unconsciousness Cough Asymptomatic (chest X-ray abnormality)

3M 11M N/A N/A Unknown

3M 11M 7–9 M Unknown

P. dehaani P. dehaani N/A N/A Unknown

Unknown

Unknown

46

45

M

Japanese

Asymptomatic (chest X-ray abnormality)

several W

7 years

dehaani dehaani dehaani dehaani

dehaani dehaani dehaani dehaani

dehaani dehaani dehaani dehaani

Eriocheir japonicus, P. dehaani P. dehaani

OCS: oral corticosteroid, M: male, F: female, N/A: not applicable, N/D: not done, CF: complement fixation, ELISA: enzyme-linked immunosorbent assay, dot-ELISA: multiple-dot enzymelinked immunosorbent assay, P. dehaani: Potamon dehaani, M: months, W: weeks, Y: years, TBLB: transbronchial lung biopsy, BALF: bronchoalveolar lavage fluid

pneumonia have to be considered as differential diagnoses. Corticosteroid treatment may delay the true diagnosis of paragonimiasis and may also affect the life cycle of paragonimiasis; therefore, aggressive approaches such as bronchoscopic examination and serological

examinations to differentiate the differential diagnoses have to be considered before starting corticosteroid treatment. It had taken about 7 years before the correct diagnosis of P. miyazakii infection was made. To the best of our knowledge,

278

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Table 2 Reported cases of P. miyazakii with the intrapulmonary involvement. Location of eating raw meet

Pulmonary involvement

Pulmonary pathology

Recovery of ova from respiratory samples

Used serological diagnostic tests

Yokohama Tokyo Tochigi Hokkaido

Rt. infiltrations Bilateral infiltrations Rt. infiltrations Lt. nodule

N/D N/D Granuloma (TBLB from lt. S6) N/D

– – – Sputum, feces

CF ELISA dot-ELISA Ouchterlony, CF

Thailand and Gunma

Bilateral nodules

N/D



dot-ELISA, microplate-ELISA

Yokohama

Lt. nodule

-

Ouchterlony

Tokyo Fukui Ibaraki

Rt. infiltrations Rt. infiltrations Nodule in rt. Lower lobe

– – –

dot-ELISA, Ouchterlony, inhibition test cystein protease antigen ELISA, Ouchterlony dot-ELISA, microplate-ELISA

Yokohama Yokohama N/A Tokyo

– – – –

CF, Ouchterlony, immunoelectrophoresis CF CF, Ouchterlony Ouchterlony, immunoelectrophoresis

N/D N/D

– –

CF, Ouchterlony CF, Ouchterlony

N/D N/D N/D N/D

– – – –

CF, Ouchterlony Immunoelectrophoresis Ouchterlony Ouchterlony

N/A N/A Akita Unknown

Rt. infiltration Rt. lower infiltration Rt. lower nodule Ground glass attenuations in rt. upper lung field, rt. patchy infiltrations Bilateral infiltrations Infiltrations in lt. upper and middle lung fields Infiltrations in lt. upper lung field Lt. lower cavitary opacities Cavitary nodular opacities Nodules and infiltrations in the rt. Upper lung field infiltration infiltration in the rt. middle lobe Lt. lower infiltration Infiltration in the rt. middle lobe

Granuloma(lt. lower lobe, transcutaneous lung biopsy) Unremarkable findings (TBLB) N/D Necrotizing granuloma with acute hemorrhagic abscess accompanying eosinophilic infiltration (rt. Lower lobe, surgical lung biopsy) N/D N/D N/D N/D

N/D N/D N/D N/D

– – – –

Immunological specific method CF, Ouchterlony Ouchterlony CF, Ouchterlony

Unknown

Infiltration in the lt. middle lung field

N/D



CF, Ouchterlony

Nagano

Rt. lower infiltration

N/D



N/A Tokyo Chiba N/A N/A N/A Osaka Unknown

N/D N/D Eosinophilic infiltration (TBLB) N/D N/D TBLB BALF Eosinophilic infiltration (TBLB, BALF) Eosinophilic infiltration (TBLB, BALF)

– – – – – – – –

N/D N/D N/D N/D N/D

– – – – –

ELISA inhibition test ELISA inhibition test Pleural fluid immunological test Specific antibody detection CF

Miyazaki

Bilateral infiltrations Rt. lower infiltration Bilateral infiltrations Infiltration N/A Infiltration Infiltrations in bilateral upper lung fields Mass shadows in the rt. upper and lt. middle lung fields Lt. lung nodule Lt. cavitary nodule Lt. lower mass Bilateral cavitary opacities Infiltration in the lt. lower lung field and nodule in the rt. middle lung field Rt. Upper lobe opacities cavity N/A N/A Bilateral infiltrations Rt. Upper lobe bronchitis Left lung nodules

ELISA, Ouchterlony, antigen-specific lymphocyte stimulation test Immunoprecipitation CF, Ouchterlony Counter current immunoelectrophoresis Immunological assessment Immunoelectrophoresis N/A Ouchterlony, CF, immunoelectrophoresis Serum and pleural fluid Ouchterlony

N/D N/D N/D N/D N/D N/D N/D

– – – – Sputum, feces – –

CF, Ouchterlony, Immunoelectrophoresis CF, Ouchterlony, Immunoelectrophoresis CF CF dot-ELISA, Ouchterlony, ELISA inhibition test CF, immunoelectrophoresis dot-ELISA, Ouchterlony, ELISA inhibition test

Mie

Bilateral infiltrations

N/D

BALF

dot-ELISA, microplate-ELISA

Yokohama Yokohama Yokohama Kyoto Yokohama Aichi

N/A N/A N/A N/A N/A Yokohama Yokohama N/A N/A Osaka

(continued on next page)

there have been no previous reports of patients with P. miyazakii infection that showed a long undiagnosed clinical course like this patient. The transfer to several hospitals after the first appearance of his clinical symptoms and the long-term corticosteroid treatment

might have been associated with this rare long clinical course of P. miyazakii infection. In summary, we herein reported a rare case of paragonimiasis caused by P. miyazakii that showed pulmonary manifestations and a

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Table 2 Table 2 (continued) Reported cases of P. miyazakii with the intrapulmonary involvement. Case no.

Treatment

OCS

Reasons of OCS treatment

1 2 3 4

Bithionol Praziquantel Praziquantel Bithionol

– – – +

5

Praziquantel



Imai H, et al. Kitakanto Med J, 61;179–185, 2011

6

Bithionol



Takahashi et al. Nippon Kyoubu Shikkan Gakkai Zasshi, 13; 169, 1975

7 8 9

Praziquantel Praziquantel Praziquantel

– – –

Katagiri S, et al. Nippon Kokyuki Gakkai Zasshi, 40; 225–229, 2002 Kojima T, et al. Nippon Kokyuki Gakkai Zasshi, 37;710–714, 1999 Ohta K, et al. Nippon Kokyuki Gakkai Zasshi, 47; 232–236, 2009

10 11 12 13

Bithionol Bithionol Bithionol Bithionol

– – – +

Suzuki S, et al. Nippon Kyoubu Rinsho, 5; 355–362, 1976 Suzuki S, et al. Nippon Kyoubu Rinsho, 5; 355–362, 1976 Takahashi T, et al. Nippon Naika Gakkai Zasshi, 65; 604, 1976 Maeda K, et al. Nippon Kyoubu Rinsho, 38;645–651, 1979

14 15

Bithionol Bithionol

– –

16 17 18 19

Bithionol Bithionol Bithionol Bithionol

– + – +

20 21 22 23

Bithionol Bithionol Bithionol Bithionol

N/A – – +

24

Bithionol



Okazaki T, et al. Nihon Iji Shinpou, 3002; 13–18, 1981

25

Bithionol



Okubo Y, et al. Nippon Naika Gakkai Zasshi, 72; 582–587, 1983

26 27 28 29 30 31 32

Bithionol Bithionol Bithionol Bithionol N/A N/A Bithionol

– + + – – – +

33

Praziquantel

+

34 35 36 37 38

N/A N/A Bithionol N/A Bithionol

– – – – –

Nawa Y, et al. Kiseichugaku Zasshi, 43; 160, 1994 Nawa Y, et al. Kiseichugaku Zasshi, 43; 160, 1994 Tanki M, et al. Nihon Ikadaigaku Zasshi, 56; 87, 1989 Ichikawa T, et al. Nippon Nouson Igakukai Zasshi, 46; 94, 1997 Wakao T, et al. Yamashi Igaku, 3; 102, 1976

39 40 41 42 43 44 45

Bithionol Bithionol N/A N/A Praziquantel Bithionol Praziquantel

– – – – +

Yokogawa M, et al. Kiseichugaku Zasshi, 23:167, 1974 Yokogawa M, et al. Kiseichugaku Zasshi, 23:167, 1974 Matsumine H, et al. Jpn J Intern Med. 74: 597–605, 1985 Matsumine H, et al. Jpn J Intern Med. 74: 597–605, 1985 Okamoto M, et al. Jpn J Parasitol. 42:429–433, 1993 Yokogawa M, et al. Kanzen, Enshou, Meneki, 48;, 1974 Ono S, et al. Jpn J Parasitol. 41:279–282, 1992

46

Praziquantel

+

Eosinophilia

Eosinophilia

Duration from OCS treatment to diagnosis of P. miyazakii

6M

4M

References Kobayashi A, et al. Jikeikai Med J, 22;127–135, 1975 Ozawa Y, et al. Iryo, 46; 634–638, 1992 Kato T, et al. Nihon Kyoubu Rinsho, 60; 672–677, 2001 Imai S, Nihon Naika Gakkai Zasshi, 76; 1881–1882, 1987

Nakamura S, Shindan to Chiryo, 63; 2147–2153, 1975 Nakamura S, Shindan to Chiryo, 63; 2147–2153, 1975

Tuberculous pleuritis

4M

Tuberculous pleuritis

7M

Nakamura S, Shindan to Chiryo, 63; 2147–2153, 1975 Matsumoto S, et al. Kyoto Furitu Ikadaigakushi, 85; 392–396, 1976 Yoshida M, et al. Kiseichugaku Zasshi, 26; 13, 1977 Ichimura K, et al. Nippon Kyoubu Rinsho, 37; 583–587, 1978

2M

Yamada N, Nippon Kyoubu Shikkann Gakkaishi, 17; 751–752, 1979 Hayakawa I, et al. Nippon Naika Gakkai Zasshi, 69; 1172, 1980 Imano T, et al. Akitaken Nouson Igakukai Zasshi, 27; 23–26, 1981 Okazaki T, et al. Nihon Iji Shinpou, 3002; 13–18, 1981

Loffler endocarditis

Eosinophilia Eosinophilia

2M 1M

Eosinophilic pneumonia, hypereosinophilic syndrome Eosinophilic pneumonia

1M

Tsuzuki N, et al. Nippon Kyoubu Shikan Gakkaishi, 22; 537, 1984 Soutsu M, et al. Noushinkeigeka, 12; 865–870, 1984 Fukuda S, et al. Aomorikenritsu Chuou Byouin Igakushi, 31; 462–466, 1986 Hatano M, et al. Nippon Kyoubu Shikkan Gakkai Zasshi, 26; 818, 1986 Yamasaki T, et al. Nippon Kyoubu Shikkan Gakkai Zasshi, 24; 346, 1986 Masaki H, et al. Nippon Kyoubu Shikkan Gakkai Zasshi, 26; 784, 1988 Yasuba H, et al. Nippon Kyoubu Rinsho, 48; 651–655, 1989

8W

Yamamoto T, et al. Nippon Kyoubu Rinsho, 53; 337–341, 1994

Allergic granulomatous angitis

6M

Eosinophilic pneumonia

7 years



long clinical course after infection. A morphological examination of the ova detected in the bronchial lavage fluid and the absorbance of IgGELISA of the patient's serum against P. miyazakii were useful for diagnosing P. miyazakii in this case.

Present patient

Conflict of interest The authors have no conflicts of interest to declare in association with this study.

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Acknowledgments We give special thanks to Prof. Haruhiko Maruyama (Division of Parasitology, Department of Infectious Diseases, Graduate School of Medicine and Veterinary Medicine, University of Miyazaki, Japan) for valuable advice. References [1] Maruyama H, Noda S, Nawa Y. Emerging problems of parasitic disease in southern Kyushu, Japan. Jpn J Parasitol 1996;45:192–200. [2] Nakamura-Uchiyama F, Hiromatsu K, Ishiwata K, Sakamoto Y, Nawa Y. The current status of parasitic diseases in Japan. Intern Med 2003;42:222–36. [3] Nakamura-Uchiyama F, Mukae H, Nawa Y. Paragonimiasis: a Japanese perspective. Clin Chest Med 2002;23:409–20. [4] Nagayasu E, Yoshida A, Hombu A, Horii Y, Maruyama H. Paragonimiasis in Japan: a twelve-year retrospective case review (2001–2012). Intern Med 2015;54:179–86. [5] Mukae H, Nakamura-Uchiyama F, Nawa Y. Pulmonary paragonimiasis and its surgical complications. In: Shields TW, editor. General Thoracic Surgery. Philadelphia: Lippincott Williams & Wilkins; 2009. p. 1197–204. [6] Blair D, Xu ZB, Agatsuma T. Paragonimiasis and the genus Paragonimus. Adv Parasitol 1999;42:113–222.

[7] Yokogawa M. Pragonimus and paragonimiasis. In: Morishita K, editor. Progress of medical parasitology in Japan. , English ed.Tokyo: Meguro Parasitological Museum; 1964. p. 63–156. [8] Matumine H, Araki K. A case of paragonimiasis miyazakii appearing with bilateral pneumothorax, effusion and alternating chest pain—a review of 82 cases reported in Japan. Nippon Naika Gakkai Zasshi 1985;74:597–605. [9] Nakamura-Uchiyama F, Onah DN, Nawa Y. Clinical features of paragonimiasis cases recently found in Japan: parasite-specific immunoglobulin M and G antibody classes. Clin Infect Dis 2001;32:e151–3. [10] Terashima T, Takeuchi E, Nishio H, Ishikawa M, Yamamoto N, Araki J, et al. A case of pulmonary paragonimiasis: isolation of adult Paragonimus miyazakii from resected lung tissue. Clin Parasitol 2009;20:43–5. [11] Imai S, Yoshida K, Nakata N, Okada H, Koba H, Suzuki A. A case of paragonimiasis miyazakii: showing worm cysts in the lung, and eggs detected from feces and sputum. Nippon Naika Gakkai Zasshi 1987;76:1881–2. [12] Yamamoto C, Yamada Y, Takezawa Y, Yoshimoto E, Ueda Y, Nishiyama T, et al. A case of paragonimiasis miyazakii with variable X-ray shadows and atypical clinical course. Nippon Kyobu Rinsho 1994;53:337–41. [13] Hashiguchi Y, Hirai H. Influence of immunosuppressants on the establishment of Paragonimus miyazakii in albino rats. J Helminthol 1977;51:87–94. [14] Kojima T, Takase K, Kasakura N. Paragonimiasis miyazakii with variable X-ray shadows. Nihon Kokyuki Gakkai Zasshi 1999;37:710–4.

A rare case of paragonimiasis miyazakii with lung involvement diagnosed 7 years after infection: A case report and literature review.

We report a rare case of pulmonary paragonimiasis caused by Paragonimus miyazakii that showed pulmonary manifestations and a long-term clinical course...
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