Parasites, Hosts and Diseases

"Paragonimus westermani"

Mini Review

Paragonimus and Paragonimiasis in Vietnam: an Update: Pham Ngoc Doanh, Yoichiro Horii, Yukifumi Nawa; Korean J Parasitol 2013;51(6):621-627.
Published online December 31, 2013; DOI: https://doi.org/10.3347/kjp.2013.51.6.621

Abstract
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Paragonimiasis is a food-borne parasitic zoonosis caused by infection with lung flukes of the genus Paragonimus. In Vietnam, research on Paragonimus and paragonimiasis has been conducted in northern and central regions of the country. Using a combination of morphological and molecular methods, 7 Paragonimus species, namely P. heterotremus, P. westermani, P. skrjabini, P. vietnamensis, P. proliferus, P. bangkokenis and P. harinasutai, have been identified in Vietnam. Of these, the first 3, P. heterotremus, P. westermani and P. skrjabini, are known to infect humans in other countries. However, in Vietnam, only P. heterotremus, found in some northern provinces, has been shown to infect humans. Even nowadays, local people in some northern provinces, such as Lai Chau and Yen Bai, are still suffering from P. heterotremus infection. In some provinces of central Vietnam, the prevalence and infection intensity of P. westermani metacercariae in freshwater crabs (the second intermediate hosts) are extremely high, but human cases have not been reported. Likewise, although P. skrjabini was found in Thanh Hoa Province, its pathogenicity to humans in Vietnam still remains uncertain. The results of molecular phylogenetic analyses of Vietnamese Paragonimus species provides new insights on the phylogeny and taxonomy of the genus Paragonimus. Comprehensive molecular epidemiological and geobiological studies on the genus in Vietnam and adjacent countries are needed to clarify the biodiversity and public health significance of the lung flukes.

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Simultaneous Paragonimus infection involving the breast and lung: A case report
Moon Young Oh, Ajung Chu, Jeong Hwan Park, Jong Yoon Lee, Eun Youn Roh, Young Jun Chai, Ki-Tae Hwang
World Journal of Clinical Cases.2019; 7(24): 4292. CrossRef
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Carolina Lenis, Alicia Galiano, Imelda Vélez, Iván Darío Vélez, Carlos Muskus, Antonio Marcilla
Acta Tropica.2018; 183: 95. CrossRef
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Pham Ngoc Doanh, Luu Anh Tu, Hoang Van Hien, Nguyen Van Duc, Yoichiro Horii, David Blair, Yukifumi Nawa
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Shasha Yu, Xilin Zhang, Wenbi Chen, Hong Zheng, Guoping Ai, Nan Ye, Ying Wang
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P.N. Doanh, H.V. Hien, L.A. Tu, N. Nonaka, Y. Horii, Y. Nawa
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Molecular and morphological variation of Paragonimus westermani in Vietnam with records of new second intermediate crab hosts and a new locality in a northern province
N. PHAM DOANH, A. LUU TU, T. DUNG BUI, T. HO LOAN, NARIAKI NONAKA, YOICHIRO HORII, DAVID BLAIR, YUKIFUMI NAWA
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Case Reports

Intestinal Paragonimiasis with Colonic Ulcer and Hematochezia in An Elderly Taiwanese Woman: Chung-Te Liu, Yen-Cheng Chen, Tso-Hsiao Chen, Ursula Barghouth, Chia-Kwung Fan; Korean J Parasitol 2012;50(4):349-352.
Published online November 26, 2012; DOI: https://doi.org/10.3347/kjp.2012.50.4.349

Abstract
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A 94-year-old female with end-stage renal disease presents with fever, fatigue, and hematochezia. She had previously resided in Hunan Province, China, and Myanmar, and she immigrated to Taiwan 30 years ago. Colonoscopy revealed a colonic ulcer. Biopsy of the colonic ulcer showed ulceration of the colonic mucosa, and many Paragonimus westermani-like eggs were noted. Serum IgG antibody levels showed strong reactivity with P. westermani excretory-secretory antigens by ELISA. Intestinal paragonimiasis was thus diagnosed according to the morphology of the eggs and serologic finding. After treatment with praziquantel, hematochezia resolved. The present case illustrates the extreme manifestations encountered in severe intestinal paragonimiasis.

Citations

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Incidental diagnosis of paragonimiasis after histopathological examination of cholecystectomy specimen in Nepal: A case report
Pearlbiga Karki, Pinky Jha, Gaurab Mainali, Manoj Khadka, Prabesh Karki, Jung Bahadur Thapa, Gayatri Karki
Annals of Medicine and Surgery.2021; 63: 102170. CrossRef
A Case of Ectopic Peritoneal Paragonimiasis Mimicking Diverticulitis or Abdominal Abscess
Min Jae Kim, Sung-Han Kim, Sang-Oh Lee, Sang-Ho Choi, Yang Soo Kim, Jun Hee Woo, Yong Sik Yoon, Kyung Won Kim, Jaeeun Cho, Jong-Yil Chai, Yong Pil Chong
The Korean Journal of Parasitology.2017; 55(3): 313. CrossRef
Current status of Paragonimus and paragonimiasis in Ecuador
Manuel Calvopiña, Daniel Romero, Byron Castañeda, Yoshihisa Hashiguchi, Hiromu Sugiyama
Memórias do Instituto Oswaldo Cruz.2014; 109(7): 849. CrossRef

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A Pulmonary Paragonimiasis Case Mimicking Metastatic Pulmonary Tumor: Ki Uk Kim, Kwangha Lee, Hye-Kyung Park, Yeon Joo Jeong, Hak Sun Yu, Min Ki Lee; Korean J Parasitol 2011;49(1):69-72.
Published online March 18, 2011; DOI: https://doi.org/10.3347/kjp.2011.49.1.69

Abstract
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Pulmonary paragonimiasis is a relatively rare cause of lung disease revealing a wide variety of radiologic findings, such as air-space consolidation, nodules, and cysts. We describe here a case of pulmonary paragonimiasis in a 27-year-old woman who presented with a 2-month history of cough and sputum. Based on chest computed tomography (CT) scans and fluorodeoxyglucose positron emission tomography (FDG-PET) findings, the patient was suspected to have a metastatic lung tumor. However, she was diagnosed as having Paragonimus westermani infection by an immunoserological examination using ELISA. Follow-up chest X-ray and CT scans after chemotherapy with praziquantel showed an obvious improvement. There have been several reported cases of pulmonary paragonimiasis mimicking lung tumors on FDG-PET. However, all of them were suspected as primary lung tumors. To our knowledge, this patient represents the first case of paragonimiasis mimicking metastatic lung disease on FDG-PET CT imaging.

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Brief Communications

Infection Status of Freshwater Crabs and Crayfish with Metacercariae of Paragonimus westermani in Korea: Eun-Min Kim, Jae-Lip Kim, Sung-Il Choi, Soon-Hyung Lee, Sung-Tae Hong; Korean J Parasitol 2009;47(4):425-426.
Published online December 2, 2009; DOI: https://doi.org/10.3347/kjp.2009.47.4.425

Abstract
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The present study investigated the infection status of Paragonimus westermani metacercariae in freshwater crabs (n = 363) and crayfish (n = 31) from October 2007 to October 2008 using the crush method. All of the freshwater crabs, Eriocheir japonicus, were negative for P. westermani metacercariae while 10 (32.3%) of the 31 examined crayfish were positive. The 10 positive crayfish were caught in Haenam, Jeollanam-do, and there were 8-59 (mean 28.4) metacrcariae per infected crayfish. These results suggest that P. westermani metacerariae are still transmitted by crayfish enzootically in southern Korea, and that freshwater crabs may transmit metacercariae only on rare occasions.

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The Korean Journal of Parasitology.2017; 55(3): 347. CrossRef
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Ah Young Kim
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Min Seo
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Chang Ho Lee, Jong Hun Kim, Woo Sung Moon, Min Ro Lee
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Eun Jung Koh, Seung-Ki Kim, Kyu-Chang Wang, Jong-Yil Chai, Sangjoon Chong, Sung-Hye Park, Jung-Eun Cheon, Ji Hoon Phi
Journal of Korean Medical Science.2012; 27(11): 1428. CrossRef
Intestinal Paragonimiasis with Colonic Ulcer and Hematochezia in An Elderly Taiwanese Woman
Chung-Te Liu, Yen-Cheng Chen, Tso-Hsiao Chen, Ursula Barghouth, Chia-Kwung Fan
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A 27 kDa Cysteine Protease Secreted by Newly Excysted Paragonimus westermani Metacercariae Induces Superoxide Anion Production and Degranulation of Human Eosinophils: Young-Bae Chung, Hirohito Kita, Myeong Heon Shin; Korean J Parasitol 2008;46(2):95-99.
Published online June 20, 2008; DOI: https://doi.org/10.3347/kjp.2008.46.2.95

Abstract
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Eosinophil degranulation plays a crucial role in tissue inflammatory reactions associated with helminth parasitic infections and allergic diseases. Paragonimus westermani, a lung fluke causing human paragonimiasis, secretes a large amount of cysteine proteases, which are involved in nutrient uptake, tissue invasion, and modulation of hos's immune responses. There is, however, limited information about the response of eosinophils to direct stimulation by cysteine proteases (CP) secreted by P. westermani. In the present study, we tested whether degranulation and superoxide production from human eosinophils can be induced by stimulation of the 2 CP (27 kDa and 28 kDa) purified from excretory-secretory products (ESP) of P. westermani newly excysted metacercariae (PwNEM). A large quantity of eosinophil-derived neurotoxin (EDN) was detected in the culture supernatant when human eosinophils isolated from the peripheral blood were incubated with the purified 27 kDa CP. Furthermore, the 27 kDa CP induced superoxide anion production by eosinophils in time- and dose-dependent manners. In contrast, the purified 28 kDa CP did not induce superoxide production and degranulation. These findings suggest that the 27 kDa CP secreted by PwNEM induces superoxide production and degranulation of human eosinophils, which may be involved in eosinophil-mediated tissue inflammatory responses during the larval migration in human paragonimiasis.

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Original Article

Molecular and biochemical characterization of hemoglobinase, a cysteine proteinase, in Paragonimus westermani: Joon-Hyuck Choi, Jae-Hyuk Lee, Hak-Sun Yu, Hae-Jin Jeong, Jin Kim, Yeon-Chul Hong, Hyun-Hee Kong, Dong-Il Chung; Korean J Parasitol 2006;44(3):187-196.
Published online September 20, 2006; DOI: https://doi.org/10.3347/kjp.2006.44.3.187

Abstract
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The mammalian trematode Paragonimus westermani is a typical digenetic parasite, which can cause paragonimiasis in humans. Host tissues and blood cells are important sources of nutrients for development, growth and reproduction of P. westermani. In this study, a cDNA clone encoding a 47 kDa hemoglobinase of P. westermani was characterized by sequencing analysis, and its localization was investigated immunohistochemically. The phylogenetic tree prepared based on the hemoglobinase gene showed high homology with hemoglobinases of Fasciola hepatica and Schistosoma spp. Moreover, recombinant P. westermani hemoglobinase degradaded human hemoglobin at acidic pH (from 3.0 to 5.5) and its activity was almost completely inhibited by E-64, a cysteine proteinase inhibitor. Immunohistochemical studies showed that P. westermani hemoglobinase was localized in the epithelium of the adult worm intestine implying that the protein has a specific function. These observations suggest that hemoglobinase may act as a digestive enzyme for acquisition of nutrients from host hemoglobin. Further investigations may provide insights into hemoglobin catabolism in P. westermani.

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Characterization and localization of antigens for serodiagnosis of human paragonimiasis
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Brief Communication

Degranulation of human eosinophils induced by Paragonimus westermani-secreted protease: Myeong Heon Shin, Young-Bae Chung, Hirohito Kita; Korean J Parasitol 2005;43(1):33-37.
Published online March 20, 2005; DOI: https://doi.org/10.3347/kjp.2005.43.1.33

Abstract
PDF

Eosinophil degranulation is considered to be a key effector function for the killing of helminthic worms and tissue inflammation at worm-infected lesion sites. However, relatively little data are available with regard to eosinophil response after stimulation with worm-secreted products which contain a large quantity of cysteine proteases. In this study, we attempted to determine whether the degranulation of human eosinophils could be induced by the direct stimulation of the excretory-secretory products (ESP) of Paragonimus westermani, which causes pulmonary paragonimiasis in human beings. Incubation of eosinophils for 3 hr with Paragonimus-secreted products resulted in marked degranulation, as evidenced by the release of eosinophil-derived neurotoxin (EDN) in the culture supernatants. Moreover, superoxide anion was produced by eosinophils after stimulation of the ESP. The ESP-induced EDN release was found to be significantly inhibited when the ESP was pretreated with protease inhibitor cocktail or the cysteine protease inhibitor, E-64. These findings suggest that human eosinophils become degranulated in response to P. westermani-secreted proteases, which may contribute to in vivo tissue inflammation around the worms.

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Original Articles

Divergent long-terminal-repeat retrotransposon families in the genome of Paragonimus westermani: Young-An Bae, Yoon Kong; Korean J Parasitol 2003;41(4):221-231.
Published online December 20, 2003; DOI: https://doi.org/10.3347/kjp.2003.41.4.221

Abstract
PDF

To gain information on retrotransposons in the genome of Paragonimus westermani, PCR was carried out with degenerate primers, specific to protease and reverse transcriptase (rt) genes of long-terminal-repeat (LTR) retrotransposons. The PCR products were cloned and sequenced, after which 12 different retrotransposon-related sequences were isolated from the trematode genome. These showed various degrees of identity to the polyprotein of divergent retrotransposon families. A phylogenetic analysis demonstrated that these sequences could be classified into three different families of LTR retrotransposons, namely, Xena, Bel, and Gypsy families. Of these, two mRNA transcripts were detected by reverse transcriptase-PCR, showing that these two elements preserved their mobile activities. The genomic distributions of these two sequences were found to be highly repetitive. These results suggest that there are diverse retrotransposons including the ancient Xena family in the genome of P. westermani, which may have been involved in the evolution of the host genome.

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Phylogenetic relationship of ribosomal ITS2 and mitochondrial COI among diploid and triploid Paragonimus westermani isolates: Gab-Man Park, Kyung-Il Im, Tai-Soon Yong; Korean J Parasitol 2003;41(1):47-55.
Published online March 20, 2003; DOI: https://doi.org/10.3347/kjp.2003.41.1.47

Abstract
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We compared patterns of intraspecific polymorphism of two markers with contrasting modes of evolution, nuclear ribosomal DNA (rDNA) and mitochondrial DNA (mtDNA), in the lung fluke, diploid and triploid Paragonimus westermani from three geographical regions of Korea. The genetic distances between three populations of Korean diploid and triploid P. westermani showed no significant difference in the nucleotide sequences of the mitochondrial cytochrome c oxidase subunit I (mtCOI) and ribosomaal second internal transcribed spacer (ITS2) genes. A highly resolved strict-consensus tree was obtained that illustrated phylogenetically useful information of the ITS2 and mtCOI sequences from diploid and triploid P. westermani.

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Excretory bladder: the source of cysteine proteases in Paragonimus westermani metacercariae: Hyun-Jong Yang, Young-Bae Chung, Shin-Yong Kang, Yoon Kong, Seung-Yull Cho; Korean J Parasitol 2002;40(2):89-92.
Published online June 30, 2002; DOI: https://doi.org/10.3347/kjp.2002.40.2.89

Abstract
PDF

The cysteine proteases of Paragonimus westermani metacercariae are involved in metacercarial excystment, host immune modulation, and possibly in tissue penetration. In order to clarify the origin of the enzymes, 28 and 27 kDa cysteine proteases in metacercarial excretory-secretory products were purified through the FPLC system using Mono Q column chromatography. The polyclonal antibodies to the enzymes were produced in BALB/c mice. Immunolocalization studies revealed that both cysteine proteases were distributed at the linings of excretory bladder and excretory concretions of the metacercariae. It was suggested that the excretory epithelium of P. westermani undertake the secretory function of metacercarial cysteine proteases, in addition to its role as a route for eliminating waste products.

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Early Cysteine Protease Activity in Excretory Bladder Triggers Metacercaria Excystment of Paragonimus westermani
Y. B. Chung, T. S. Kim, H. J. Yang
Journal of Parasitology.2005; 91(4): 953. CrossRef