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AJR 2005; 185:616-621
© American Roentgen Ray Society

Clinical Observations

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
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
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
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
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).

 

Materials and Methods
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 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
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. 1C —45-year-old man with pleuropulmonary paragonimiasis. Positive tumor uptake (maximum standardized uptake value, 8.1) is seen on FDG PET.

 



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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)

 
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)

 

Results
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 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
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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  		Fig. 3B —43-year-old woman with pleuropulmonary paragonimiasis. CT scan at lung window setting shows poorly defined subpleural mass with adjacent areas of ground-glass attenuation.

 
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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  		Fig. 4B —44-year-old man with pleuropulmonary paragonimiasis. CT scan obtained 4 months after A shows diffuse thickening of pleura (arrowheads) and extrapleural fat (arrows).

 
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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  		Fig. 6B —42-year-old woman with pleuropulmonary paragonimiasis. Lung window image shows 7-mm-thick, peripheral tubular structure (arrow) that suggests worm migration track (burrow track).

 

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  		TABLE 1 : CT Features of Pulmonary Nodules in 31 Patients with Pleuropulmonary Paragonimiasis

 

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  		TABLE 2 : Other CT Findings Associated with Pulmonary Nodules in 31 Patients with Pleuropulmonary Paragonimiasis

 

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
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
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.


References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Yokogawa M. Paragonimus and paragonimiasis. Adv Parasitol 1965; 3:99 -158[Medline]
  2. Hiratsuka T, Ihi T, Kyoraku Y, Kumamoto K, Iiboshi H, Nakamura F. A case of Paragonimiasis westermani with a worm migration track on chest CT [in Japanese]. Nihon Kokyuki Gakkai Zasshi2004; 42:463 -467[Medline]
  3. Im JG, Whang HY, Kim WS, Han MC, Shim YS, Cho SY. Pleuropulmonary paragonimiasis: radiologic findings in 71 patients. AJR 1992; 159:39 -43[Abstract/Free Full Text]
  4. Im JG, Kong Y, Shin YM, et al. Pulmonary paragonimiasis: clinical and experimental studies. RadioGraphics1993; 13:575 -586[Abstract]
  5. Mukae H, Taniguchi H, Matsumoto N, et al. Clinicoradiologic features of pleuropulmonary Paragonimus westermani on Kyusyu Island, Japan. Chest 2001;120 : 514-520[Abstract/Free Full Text]
  6. Singcharoen T, Silprasert W. CT findings in pulmonary paragonimiasis. J Comput Assist Tomogr1987; 11:1101 -1102[Medline]
  7. Doutsu Y, Taniguchi H, Ashitani J, et al. A case of Paragonimiasis westermani diagnosed on the observation of parasitic ova in bronchial washing fluid and successfully treated with praziquantel [in Japanese]. Kansenshogaku Zasshi 1993;67 : 491-495[Medline]
  8. Matsumoto S, Mori H, Miyake H, et al. CT findings of pulmonary Paragonimiasis westermani [in Japanese]. Nippon Igaku Hoshasen Gakkai Zasshi 1993;53 : 565-571[Medline]
  9. Tokojima M, Mukae H, Sano A, et al. Clinical features in twenty-three patients with Paragonimiasis westermani [in Japanese]. Nihon Kokyuki Gakkai Zasshi 2001;39 : 910-914[Medline]
  10. Waite RJ, Carbonneau RJ, Balikian JP, Umali CB, Pezzella AT, Nash G. Parietal pleural changes in empyema: appearances at CT. Radiology 1990;175 : 145-150[Abstract/Free Full Text]
  11. Watanabe S, Nakamura Y, Kariatsumari K, et al. Pulmonary paragonimiasis mimicking lung cancer on FDG-PET imaging. Anticancer Res 2003; 23:3437 -3440[Medline]

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