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 Table of Contents  
CASE REPORT
Year : 2018  |  Volume : 4  |  Issue : 2  |  Page : 173-177

Delayed diagnosis of paragonimiasis in Southeast Asian immigrants: A need for global awareness


1 Department of Surgery, Summa Health, Akron, Ohio, USA
2 Cardiothoracic Surgery, Akron City Hospital, Akron, Ohio, USA

Date of Submission16-Jan-2018
Date of Acceptance16-Feb-2018
Date of Web Publication30-Aug-2018

Correspondence Address:
Dr. Michael S Firstenberg
Summa Health Medical Group, Cardiothoracic Surgery Specialists, 75 Arch Street, Suite 407, Akron, OH 44304
USA
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/IJAM.IJAM_2_18

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  Abstract 


Paragonimiasis is a food-borne parasitic infection that commonly affects humans after ingestion of raw or undercooked crustaceans. The disease is caused by lung flukes of the genus Paragonimus, which is endemic to Southeast Asia. In this report, we describe two cases of paragonimiasis diagnosed in North American immigrants from Southeast Asia. The first patient presented with a 5-year history of hemoptysis. The second presented with a 3-week history of productive cough. Both patients were initially treated with antibiotics for presumed pneumonia. The inciting pathogen was not identified by blood, sputum, or stool analyses. Ultimately, surgical resection was required, leading to the diagnosis of paragonimiasis. In the United States and other nonendemic areas, the diagnosis of paragonimiasis is often delayed due to its rarity. Increased awareness and inclusion in differential diagnoses, especially in patients originating from endemic areas, may prevent diagnostic delay and associated morbidity.
The following core competencies are addressed in this article: Practice-based learning and improvement, Medical knowledge, and Patient care.

Keywords: Immigrants, lung fluke, paragonimiasis


How to cite this article:
Eapen S, Espinal E, Firstenberg MS. Delayed diagnosis of paragonimiasis in Southeast Asian immigrants: A need for global awareness. Int J Acad Med 2018;4:173-7

How to cite this URL:
Eapen S, Espinal E, Firstenberg MS. Delayed diagnosis of paragonimiasis in Southeast Asian immigrants: A need for global awareness. Int J Acad Med [serial online] 2018 [cited 2018 Dec 11];4:173-7. Available from: http://www.ijam-web.org/text.asp?2018/4/2/173/240131




  Introduction Top


Paragonimiasis is a parasitic disease caused by ingestion of freshwater crab or crayfish infected with lung flukes of the genus Paragonimus.[1],[2] The infection is most commonly seen in immigrants from Southeast Asia, Africa, and Central and South America.[1],[3],[4] The clinical presentation is nonspecific, characterized by fever, productive cough, hemoptysis, and unintentional weight loss.[1],[3],[4],[5] These symptoms mimic those of pneumonia, tuberculosis, and malignancy.[1],[3],[4] The radiologic features overlap as well.[1],[3] An additional challenge to the clinical diagnosis is the limited availability of serologic testing. We present two cases of paragonimiasis in Southeast Asian immigrants diagnosed after failure of medical management, which necessitated surgical lung resection. Informed consent was obtained before case presentation.


  Case Reports Top


Case 1

A 21-year-old male immigrant from Myanmar presented with a 5-year history of intermittent hemoptysis. He denied associated fevers, chills, night sweats, and unintentional weight loss. He reported consumption of freshwater crab and wild boar while in Myanmar. He had undergone tuberculin skin testing, sputum testing for acid-fast bacilli, and serum interferon-gamma release assays, all of which were negative. His serum and sputum had tested negative for bacteria, viruses, fungi, and parasites. His antinuclear antibody and antineutrophil cytoplasmic antibody levels were within normal limits as well.

On physical examination, he had coarse breath sounds and rales over the right lower lung field. His complete blood count was significant for eosinophilia of 9.6% and a white blood cell count within normal limits. Chest radiography demonstrated right lower lobe nodules and cavitary lesions [Figure 1]a and [Figure 1]b. Subsequent chest computed tomography (CT) revealed multiple nodules and airspace consolidation in the right lower lobe [Figure 2]a and [Figure 2]b. CT findings prompted antibiotic therapy for pneumonia. Due to failure of medical management, the patient required a thoracotomy and right lower lobectomy. Surgical pathology demonstrated chronic inflammation and necrotizing granulomas. Associated parasitic organisms were morphologically consistent with Paragonimus westermani [Figure 3]a and [Figure 3]b. Pathology findings prompted treatment with praziquantel, which led to symptom resolution.
Figure 1: (a and b) Chest radiograph with right lower lobe nodules and cavitary lesions

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Figure 2: (a and b) Computed tomography with multiple nodules and airspace consolidation in the right lower lobe

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Figure 3: (a and b) Lung tissue with chronic inflammation and necrotizing granulomas. Associated parasitic organisms morphologically consistent with Paragonimus species. (a) ×10, (b) ×40

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Case 2

A 36-year-old male immigrant from Myanmar presented with a 3-week history of cough productive of rust-colored sputum. He had associated malaise and chills. He had been treated for pulmonary tuberculosis 3 years prior and reported eating freshwater crab and crayfish while in Myanmar. The results of serum, sputum, and stool testing for bacteria, viruses, fungi, and parasites were negative. Sputum testing for acid-fast bacilli was negative as well. His interferon-gamma release assay was weakly positive, which was expected given his remote history of tuberculosis.[6]

On presentation, his physical examination was significant for wheezes and rhonchi of the left middle lung field. His complete blood count demonstrated eosinophilia of 8.2% and a white blood cell count within normal limits. Chest radiography revealed bilateral pleural effusions and left middle and lower lobe infiltrative and atelectatic densities [Figure 4]. A cavitary infiltrative process in the medial portion of the right lower lobe was appreciated [Figure 4]. Subsequent chest CT revealed a 3.4 cm × 2.2 cm cavitary lesion of the right middle lobe with a surrounding reticulonodular infiltrate [Figure 5]a and [Figure 5]b. Left basilar atelectasis and effusion were seen as well [Figure 5]a and [Figure 5]b.
Figure 4: Chest radiograph with bilateral pleural effusions and left middle and lower lobe infiltrative and atelectatic densities. Associated cavitary infiltrative process in the right lower lobe

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Figure 5: (a and b) Computed tomography with a 3.4 cm × 2.2 cm cavitary lesion of the right middle lobe with surrounding reticulonodular infiltrate. Left basilar atelectasis and effusion

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Due to persistent symptoms despite 2 weeks of broad-spectrum antibiotic therapy, the patient underwent thoracotomy and wedge resection of the right middle lobe. Surgical pathology revealed inflammation and parasitic eggs, consistent with P. westermani [Figure 6]a and [Figure 6]b. His symptoms resolved following treatment with praziquantel.
Figure 6: (a and b) Inflamed lung tissue with parasitic eggs consistent with Paragonimus westermani. Background acute and chronic inflammation, abscess formation, and giant-cell reaction. (a) ×4, (b) ×40

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  Discussion Top


Paragonimiasis is a food-borne parasitic infection caused by ingestion of raw or undercooked crustaceans containing lung flukes of the genus Paragonimus.[1],[2],[4],[5],[7]Paragonimiasis is considered endemic to Southeast Asia, Africa, and Central and South America.[1],[3],[4],[5] It is extremely rare in the United States, with only 35 cases reported from 1910 to 2009.[4] The earliest case of paragonimiasis in the United States was reported in 1910 in a patient who had ingested raw or undercooked crayfish.[4] In the 1970s and 1980s, most cases of paragonimiasis in the United States were reported in refugees from Southeast Asia.[4]

Nineteen of the thirty-five reported cases of paragonimiasis were attributed to P. westermani, while the remaining cases were caused by Paragonimus kellicotti, Paragonimus mexicanus, or anunspecified Paragonimus species.[4] While there are over thirty species of Paragonimus worldwide, most cases in Southeast Asia are caused by P. westermani.[5] The only lung fluke species indigenous to the United States is P. kellicotti, which is found in the Mississippi River Basin.[5]

As outlined by the United States Centers for Disease Control, the life cycle of Paragonimus begins with trematodal eggs excreted in human sputum or feces.[8] The eggs embryonate and hatch as larvae.[8] The larvae penetrate snails, which serve as the first intermediate host.[8] Several transformations result in cercariae, which are shed in freshwater.[8] The cercariae invade freshwater crustaceans, namely crab and crayfish, which serve as second intermediate hosts.[8] While hosted by crustaceans, cercariae transform into infective metacercariae.[8] These metacercariae are consumed by reservoir hosts, which include wild boar, dogs, cats, and mongooses.[8]

Humans then ingest intermediate or reservoir hosts and become infected with metacercariae.[8] The metacercariae undergo excystation in the duodenum, pass through the intestinal wall, and penetrate the peritoneum, diaphragm, and parietal pleura.[8] After maturation in the lungs, adult flukes encapsulate in pairs and release eggs into the bronchioles.[8] These eggs are then expectorated in sputum or ingested to be excreted in feces.[8]

Paragonimiasis manifests with fever, chronic cough productive of rust-colored sputum, and hemoptysis.[1],[2],[3],[4],[5],[7] Patients may develop prodromal symptoms of abdominal pain and diarrhea during larval migration through the duodenum.[5],[7] An incubation period of 2–16 weeks is required before the development of systemic and pulmonary symptoms.[5],[7]

In a retrospective review of radiographic findings in 71 cases of paragonimiasis, 83% presented with pulmonary lesions.[9] These included patchy airspace consolidation, cystic changes, ring shadows, nodules, and peripheral linear opacities.[9],[10] Pleural lesions were seen in 61% of cases and included effusions, pleural thickening, and hydropneumothoraces.[9],[10] Chest CT findings included round cystic lesions filled with fluid or gas, centrilobular nodules, worm migration tracts, and intracystic worms.[9],[10],[11]

In a retrospective review of 36 cases of pulmonary paragonimiasis, 92% of the initial diagnoses were incorrect.[3] The incorrect diagnoses included tuberculosis, malignancy, bronchiectasis, pulmonary infiltration with eosinophilia syndrome, and chronic bronchitis.[3] Only 8% of patients were correctly diagnosed with paragonimiasis at initial presentation.[3]

The definitive diagnosis of paragonimiasis is made by finding brown, ovoid eggs in sputum, bronchoalveolar lavage, or stool samples.[2],[4],[5],[7] However, false negative sampling may occur.[1],[3] The sensitivity of single sputum examination is limited, ranging from 30% to 40%.[5] Serologic testing may establish the diagnosis of paragonimiasis when eggs are not seen in sputum, bronchoalveolar lavage, or stool samples.[1],[4] The enzyme-linked immunosorbent assay test, an immunoserologic test for Paragonimus-specific IgG antibody, is highly sensitive and specific in the diagnosis of paragonimiasis.[1],[5],[7] Serologic tests are limited by availability, and due to the rarity of disease, they are often regarded as confirmatory tests after the organisms have been identified by pathology.[1]

In the cases reported, herein, the diagnosis of paragonimiasis was made following surgical resection. Pulmonary tuberculosis and pneumonia could not be excluded at presentation given immigration from endemic areas and radiologic findings. Peripheral eosinophilia may have served as an early indication of a parasitic process in both cases.[1],[2],[4],[5],[7]

The treatment of paragonimiasis consists of a 2- to 3-day course of weight-based praziquantel.[1],[4],[5],[7] The cure rate approaches 100% following treatment.[1],[5] An effective alternative to praziquantel is triclabendazole, which is not routinely available in the United States.[5]


  Conclusion Top


With a nonspecific clinical presentation, paragonimiasis often poses a diagnostic dilemma. With increased immigration from endemic areas, it is imperative that paragonimiasis is considered and recognized early in this patient population. Immigrants reporting consumption of raw or undercooked crustaceans are at higher risk.[1],[2],[7] Eosinophilia should raise suspicion for a parasitic process as well.[1],[2],[4],[5]

Chest radiographs and CT imaging may reveal characteristic nodules, cavitary lesions, or migration tracks.[9],[10],[11] If available, serologic testing should be performed given the high false negative rate of sputum, bronchoalveolar lavage, and stool sampling.[1] Once the diagnosis is confirmed, treatment with praziquantel should be initiated.[1] Patient education is essential to the prevention of paragonimiasis.[5] Handwashing and avoiding consumption of raw or undercooked crustaceans may reduce the risk of future infection.[4],[5]

Declaration of patient consent

The authors certify that they have obtained appropriate patient consent forms. The patients have given their consent for their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

Ethical conduct of research

This literature review was conducted ethically, including appropriate pre-publication permissions from patients.



 
  References Top

1.
Lee S, Yu Y, An J, Lee J, Son JS, Lee YK, et al. A case of delayed diagnosis of pulmonary paragonimiasis due to improvement after anti-tuberculosis therapy. Tuberc Respir Dis (Seoul) 2014;77:178-83.  Back to cited text no. 1
    
2.
Kalhan S, Sharma P, Sharma S, Kakria N, Dudani S, Gupta A, et al. Paragonimus westermani infection in lung: A confounding diagnostic entity. Lung India 2015;32:265-7.  Back to cited text no. 2
[PUBMED]  [Full text]  
3.
Jeon K, Koh WJ, Kim H, Kwon OJ, Kim TS, Lee KS, et al. Clinical features of recently diagnosed pulmonary paragonimiasis in Korea. Chest 2005;128:1423-30.  Back to cited text no. 3
    
4.
Fried B, Abruzzi A. Food-borne trematode infections of humans in the United States of America. Parasitol Res 2010;106:1263-80.  Back to cited text no. 4
    
5.
Diaz, JH. Paragonimiasis acquired in the United States: Native and nonnative species. Clin Microbiol Rev 2013;26:493-504.  Back to cited text no. 5
    
6.
Gamsky TE, Lum T, Hung-Fan M, Green JA. Cumulative false-positive quantiFERON-TB interferon-γ release assay results. Ann Am Thorac Soc2016;13:660-5.  Back to cited text no. 6
    
7.
Centers for Disease Control and Prevention (CDC). Human paragonimiasis after eating raw or undercooked crayfish - Missouri, July 2006-September 2010. MMWR Morb Mortal Wkly Rep 2010;59:1573-6.  Back to cited text no. 7
    
8.
CDC – Global Health – Division of Parasitic Diseases. Paragonimiasis – Biology. Available from: https://www.cdc.gov/parasites/paragonimus/biology.html. [Last accessed on 2017 Dec 17].  Back to cited text no. 8
    
9.
Im JG, Whang HY, Kim WS, Han MC, Shim YS, Cho SY, et al. Pleuropulmonary paragonimiasis: Radiologic findings in 71 patients. AJR Am J Roentgenol 1992;159:39-43.  Back to cited text no. 9
    
10.
Kim TS, Han J, Shim SS, Jeon K, Koh WJ, Lee I, et al. Pleuropulmonary paragonimiasis: CT findings in 31 patients. AJR Am J Roentgenol 2005;185:616-21.  Back to cited text no. 10
    
11.
Kuroki M, Hatabu H, Nakata H, Hashiguchi N, Shimizu T, Uchino N, et al. High-resolution computed tomography findings of P. westermani. J Thorac Imaging 2005;20:210–3.  Back to cited text no. 11
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]



 

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