Parasites, Hosts and Diseases

"Paragonimus"

Brief Communication

Evaluation of IgG4 Subclass Antibody Detection by Peptide-Based ELISA for the Diagnosis of Human Paragonimiasis Heterotrema: Pewpan M. Intapan, Oranuch Sanpool, Penchom Janwan, Porntip Laummaunwai, Nimit Morakote, Yoon Kong, Wanchai Maleewong; Korean J Parasitol 2013;51(6):763-766.
Published online December 31, 2013; DOI: https://doi.org/10.3347/kjp.2013.51.6.763

Abstract
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A synthetic peptide was prepared based on the antigenic region of Paragonimus westermani pre-procathepsin L, and its applicability for immunodiagnosis for human paragonimiasis (due to Paragonimus heterotremus) was tested using an ELISA to detect IgG4 antibodies in the sera of patients. Sera from other helminthiases, tuberculosis, and healthy volunteers were used as the references. This peptide-based assay system gave sensitivity, specificity, accuracy, and positive and negative predictive values of 100%, 94.6%, 96.2%, 100%, and 88.9%, respectively. Cross reactivity was frequently seen against the sera of fascioliasis (75%) and hookworm infections (50%). Since differential diagnosis between paragonimiasis and fascioliasis can be easily done by clinical presentation and fascioliasis serology, this cross reaction is not a serious problem. Sera from patients with other parasitoses (0-25%) rarely responded to this synthetic antigen. This synthetic peptide antigen seems to be useful for development of a standardized diagnostic system for paragonimiasis.

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An immunochromatographic test using whole blood for rapid diagnosis of human paragonimiasis and its diagnostic usefulness
Patcharaporn Boonroumkaew, Lakkhana Sadaow, Penchom Janwan, Rutchanee Rodpai, Oranuch Sanpool, Tongjit Thanchomnang, Hiroshi Yamasaki, Pewpan M. Intapan, Wanchai Maleewong
Food and Waterborne Parasitology.2024; 37: e00246. CrossRef
Development of point-of-care testing tool using immunochromatography for rapid diagnosis of human paragonimiasis
Lakkhana Sadaow, Oranuch Sanpool, Hiroshi Yamasaki, Wanchai Maleewong, Pewpan M. Intapan
Acta Tropica.2020; 203: 105325. CrossRef
Paragonimus and paragonimiasis in Asia: An update
Ayako Yoshida, Pham Ngoc Doanh, Haruhiko Maruyama
Acta Tropica.2019; 199: 105074. CrossRef
A Case of Pulmonary Paragonimiasis with Chronic Abdominal Pain and Erythematous Rash in a 6-year-old Girl
Ju Young Kim, Min Kyu Park, Yong Ju Lee, Sun Huh, Ky Young Cho
Pediatric Infection and Vaccine.2018; 25(1): 54. CrossRef
A tool for mass-screening of paragonimiasis: an enzyme-linked immunosorbent assay with urine samples
Xu Guang Qiu, Fukumi Nakamura-Uchiyama, Yukifumi Nawa, Makoto Itoh
Tropical Medicine and Health.2016;[Epub] CrossRef
Expression characteristics and specific antibody reactivity of diverse cathepsin F members of Paragonimus westermani
Chun-Seob Ahn, Byoung-Kuk Na, Dong-ll Chung, Jeong-Geun Kim, Jin-Taek Kim, Yoon Kong
Parasitology International.2015; 64(1): 37. CrossRef
North American paragonimiasis: epidemiology and diagnostic strategies
Peter U Fischer, Gary J Weil
Expert Review of Anti-infective Therapy.2015; 13(6): 779. CrossRef

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Original Articles

Paragonimus paishuihoensis Metacercariae in Freshwater Crabs, Potamon lipkei, in Vientiane Province, Lao PDR: Shigehisa Habe, Pham Ngoc Doanh, Shinichiro Yahiro, Nanthasane Vannavong, Hubert Barennes, Peter Odermatt, Gilles Dreyfuss, Yoichiro Horii, Yukifumi Nawa; Korean J Parasitol 2013;51(6):683-687.
Published online December 31, 2013; DOI: https://doi.org/10.3347/kjp.2013.51.6.683

Abstract
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Among Paragonimus species, P. paishuihoensis is one of the most mysterious and poorly understood species. Metacercariae are characterized by having a unique dendritically branched excretory bladder. However, the morphology of the adult worm remains unknown. To date, metacercariae of this species have been reported only in China and Thailand. In this study, we first found P. paishuihoensis metacercariae in freshwater crabs, Potamon lipkei, in Hinheub District, Vientiane, Lao PDR, with a prevalence of 77.7% and the average intensity of 10.3 (range 1-28) metacercariae per crab. The molecular data based on ITS2 and CO1 markers indicated that P. paishuihoensis from Laos and Thailand were almost completely identical and were close to members of the Paragonimus bangkokensis/Paragonimus harinasutai complex. Attempts to infect experimental animals (cats, dogs, and rats) with P. paishuihoensis were unsuccessful, suggesting that these animals might be unsuitable definitive hosts for the species. Further studies are necessary to elucidate the taxonomic status and life cycle of P. paishuihoensis.

Citations

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Lung flukes of the genusParagonimus: ancient and re-emerging pathogens
David Blair
Parasitology.2022; 149(10): 1286. CrossRef
Paragonimus and paragonimiasis in Asia: An update
Ayako Yoshida, Pham Ngoc Doanh, Haruhiko Maruyama
Acta Tropica.2019; 199: 105074. CrossRef
Morphological and molecular identification of a lung fluke, Paragonimus macrorchis (Trematoda, Paragonimidae), found in central Lao PDR and its molecular phylogenetic status in the genus Paragonimus
Oranuch Sanpool, Pewpan Maleewong Intapan, Tongjit Thanchomnang, Penchom Janwan, Sakhone Laymanivong, Hiromu Sugiyama, Wanchai Maleewong
Parasitology International.2015; 64(6): 513. CrossRef

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Molecular Variation in the Paragonimus heterotremus Complex in Thailand and Myanmar: Oranuch Sanpool, Pewpan M. Intapan, Tongjit Thanchomnang, Penchom Janwan, Yukifumi Nawa, David Blair, Wanchai Maleewong; Korean J Parasitol 2013;51(6):677-681.
Published online December 31, 2013; DOI: https://doi.org/10.3347/kjp.2013.51.6.677

Abstract
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Paragonimiasis is an important food-borne parasitic zoonosis caused by infection with lung flukes of the genus Paragonimus. Of the 7 members of the genus known in Thailand until recently, only P. heterotremus has been confirmed as causing human disease. An 8th species, P. pseudoheterotremus, has recently been proposed from Thailand, and has been found in humans. Molecular data place this species as a sister species to P. heterotremus, and it is likely that P. pseudoheterotremus is not specifically distinct from P. heterotremus. In this study, we collected metacercariae of both nominal species (identification based on metacercarial morphology) from freshwater crabs from Phetchabun Province in northern Thailand, Saraburi Province in central Thailand, and Surat Thani Province in southern Thailand. In addition, we purchased freshwater crabs imported from Myanmar at Myawaddy Province, western Thailand, close to the Myanmar-Thailand border. The DNAs extracted from excysted metacercariae were PCR-amplified and sequenced for ITS2 and cox1 genes. The ITS2 sequences were nearly identical among all samples (99-100%). Phylogenies inferred from all available partial cox1 sequences contained several clusters. Sequences from Indian P. heterotremus formed a sister group to sequences from P. pseudoheterotremus-type metacercariae. Sequences of P. heterotremus from Thailand, Vietnam, and China formed a separate distinct clade. One metacercaria from Phitsanulok Province was distinct from all others. There is clearly considerable genetic variation in the P. heterotremus complex in Thailand and the form referred to as P. pseudoheterotremus is widely distributed in Thailand and the Thai-Myanmar border region.

Citations

Citations to this article as recorded by

Considerable genetic diversity within Paragonimus heterotremus in Luang Prabang, northern Lao People's Democratic Republic
Alongkorn Nonthapa, Rutchanee Rodpai, Tongjit Thanchomnang, Patcharaporn Boonroumkaew, Lakkhana Sadaow, David Blair, Pewpan M. Intapan, Wanchai Maleewong, Virasack Banouvong, Sakhone Laymanivong, Oranuch Sanpool
Infection, Genetics and Evolution.2025; 128: 105718. CrossRef
Nuclear ribosomal transcription units in Asian Paragonimus species (Paragonimidae: Platyhelminthes): genetic characteristics, polymorphism, and implications for intersuperfamilial phylogeny
Khue Thi Nguyen, Huong Thi Thanh Doan, Linh Thi Khanh Pham, Do Thi Roan, Takeshi Agatsuma, Pham Ngoc Doanh, Thanh Hoa Le
Parasitology Research.2024;[Epub] CrossRef
Morphological and Molecular Characterization of Paragonimus skrjabini Complex from Yunnan, China: A Brief Report
Qiu-Hong Shu, Shu-De Li, Ming Tian, Yong Meng, Shu-Mei-Qi He, Min Zhu, Miao-Miao Wang, Wen-Lin Wang
Acta Parasitologica.2022; 67(1): 316. CrossRef
The potential use of mitochondrial ribosomal genes (12S and 16S) in DNA barcoding and phylogenetic analysis of trematodes
Abigail Hui En Chan, Naowarat Saralamba, Sompob Saralamba, Jiraporn Ruangsittichai, Urusa Thaenkham
BMC Genomics.2022;[Epub] CrossRef
General overview of the current status of human foodborne trematodiasis
Jong-Yil Chai, Bong-Kwang Jung
Parasitology.2022; 149(10): 1262. CrossRef
Genetic differentiation of Southeast Asian Paragonimus Braun, 1899 (Digenea: Paragonimidae) and genetic variation in the Paragonimus heterotremus complex examined by nuclear DNA sequences
Chairat Tantrawatpan, Sumonta Tapdara, Takeshi Agatsuma, Oranuch Sanpool, Pewpan M. Intapan, Wanchai Maleewong, Weerachai Saijuntha
Infection, Genetics and Evolution.2021; 90: 104761. CrossRef
An outbreak of Paragonimus westermani infection among Cambodian technical intern trainees in Japan, exhibiting various extrapulmonary lesions
Yoshifumi Nakagawa, Yuki Ikematsu, Takayuki Nakanishi, Yuji Ogawa, Ryuichi Taen, Yasunori Nakashima, Hironao Okabe, Ayako Yoshida, Haruhiko Maruyama
Parasitology International.2021; 81: 102279. CrossRef
Development of point-of-care testing tool using immunochromatography for rapid diagnosis of human paragonimiasis
Lakkhana Sadaow, Oranuch Sanpool, Hiroshi Yamasaki, Wanchai Maleewong, Pewpan M. Intapan
Acta Tropica.2020; 203: 105325. CrossRef
Paragonimus and paragonimiasis in Asia: An update
Ayako Yoshida, Pham Ngoc Doanh, Haruhiko Maruyama
Acta Tropica.2019; 199: 105074. CrossRef
Morphological and molecular characterization of Paragonimus caliensis Little, 1968 (Trematoda: Paragonimidae) from Medellin and Pichinde, Colombia
Carolina Lenis, Alicia Galiano, Imelda Vélez, Iván Darío Vélez, Carlos Muskus, Antonio Marcilla
Acta Tropica.2018; 183: 95. CrossRef
Gene diversity and genetic variation in lung flukes (genusParagonimus)
David Blair, Yukifumi Nawa, Makedonka Mitreva, Pham Ngoc Doanh
Transactions of The Royal Society of Tropical Medicine and Hygiene.2016; 110(1): 6. CrossRef
A review on the molecular characterization of digenean parasites using molecular markers with special reference to ITS region
K. Choudhary, A. Kumar Verma, S. Swaroop, N. Agrawal
Helminthologia.2015; 52(3): 167. CrossRef

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Ultrastructure of Spermatogenesis in the Testis of Paragonimus heterotremus: Nongnut Uabundit, Pipatphong Kanla, Phongphithak Puthiwat, Channarong Arunyanart, Kowit Chaiciwamongkol, Wanchai Maleewong, Pewpan M. Intapan, Sitthichai Iamsaard, Wiphawi Hipkaeo; Korean J Parasitol 2013;51(6):669-676.
Published online December 31, 2013; DOI: https://doi.org/10.3347/kjp.2013.51.6.669

Abstract
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Lung fluke, Paragonimus heterotremus, is a flatworm causing pulmonary paragonimiasis in cats, dogs, and humans in Southeast Asia. We examined the ultrastructure of the testis of adult P. heterotremus with special attention to spermatogenesis and spermiogenesis using scanning and transmission electron microscopy. The full sequence of spermatogenesis and spermiogenesis, from the capsular basal lamina to the luminal surface, was demonstrated. The sequence comprises spermatogonia, spermatocytes with obvious nuclear synaptonemal complexes, spermatids, and eventual spermatozoa. Moreover, full steps of spermatid differentiation were shown which consisted of 1) early stage, 2) differentiation stage representing the flagella, intercentriolar body, basal body, striated rootlets, and electron dense nucleus of thread-like lamellar configuration, and 3) growing spermatid flagella. Detailed ultrastructure of 2 different types of spermatozoa was also shown in this study.

Citations

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Molecular identification of the trematode P. ichunensis stat. n. from lungs of siberian tigers justified reappraisal of Paragonimus westermani species complex
Anastasia N. Voronova, Konstantin S. Vainutis, Tatiana V. Tabakaeva, Mikhail V. Sapotsky, Nadezhda N. Kakareka, Yury G. Volkov, Irina V. Galkina, Mikhail Yu. Shchelkanov
Journal of Parasitic Diseases.2022; 46(3): 744. CrossRef

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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.

Citations

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Paragonimiasis in Southeast Asia: A 60-Year Bibliometric Analysis (1963–2023)
Harley M. Rodriguez, Jose Ma. M. Angeles
Acta Parasitologica.2025;[Epub] CrossRef
An overview of human helminthioses in Vietnam: Their prevention, control and lessons learnt
Hung Manh Nguyen, Dung Trung Do, Stephen E. Greiman, Ha Van Nguyen, Hien Van Hoang, Toan Quoc Phan, Phuc Pham-Duc, Henry Madsen
Acta Tropica.2023; 238: 106753. CrossRef
Lung flukes of the genusParagonimus: ancient and re-emerging pathogens
David Blair
Parasitology.2022; 149(10): 1286. CrossRef
General overview of the current status of human foodborne trematodiasis
Jong-Yil Chai, Bong-Kwang Jung
Parasitology.2022; 149(10): 1262. CrossRef
Spectrum of pleuropulmonary paragonimiasis: An analysis of 685 cases diagnosed over 22 years
Chun-Seob Ahn, Jong Wook Shin, Jeong-Geun Kim, Weon-Young Lee, Insug Kang, Jung-Gi Im, Yoon Kong
Journal of Infection.2021; 82(1): 150. CrossRef
Pleural lump after paragonimiasis treated by thoracoscopy: A case report
Yue Xie, Ya-Rui Luo, Meng Chen, Yi-Min Xie, Chen-Yu Sun, Qiang Chen
World Journal of Clinical Cases.2021; 9(3): 666. CrossRef
Paragonimus and its hosts in China: An update
Xiao-Juan Zhou, Qian Yang, Qi-Hong Tan, Li-Yanyang Zhang, Lin-Bo Shi, Jie-Xin Zou
Acta Tropica.2021; 223: 106094. CrossRef
Paragonimiasis (invasion by pulmonary flukes)
S. B. Chuelov, A. L. Rossina
CHILDREN INFECTIONS.2021; 20(3): 48. CrossRef
Molecular identification of morphologically similar microcercous cercariae of two trematode families, Paragonimidae and Troglotrematidae, concurrently found in the same snail species of the subfamily Triculinae
Pham Ngoc Doanh, Hoang Van Hien, Bui Thi Dung
Folia Parasitologica.2020;[Epub] CrossRef
Paragonimiasis: A missed diagnosis from Nepal
Shreya Shrivastav, Anamika Jha
Respiratory Medicine Case Reports.2020; 31: 101298. CrossRef
Paragonimus and paragonimiasis in Asia: An update
Ayako Yoshida, Pham Ngoc Doanh, Haruhiko Maruyama
Acta Tropica.2019; 199: 105074. CrossRef
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
Morphological and molecular characterization of Paragonimus caliensis Little, 1968 (Trematoda: Paragonimidae) from Medellin and Pichinde, Colombia
Carolina Lenis, Alicia Galiano, Imelda Vélez, Iván Darío Vélez, Carlos Muskus, Antonio Marcilla
Acta Tropica.2018; 183: 95. CrossRef
First intermediate hosts of Paragonimus spp. in Vietnam and identification of intramolluscan stages of different Paragonimus species
Pham Ngoc Doanh, Luu Anh Tu, Hoang Van Hien, Nguyen Van Duc, Yoichiro Horii, David Blair, Yukifumi Nawa
Parasites & Vectors.2018;[Epub] CrossRef
A Case of Pulmonary Paragonimiasis with Chronic Abdominal Pain and Erythematous Rash in a 6-year-old Girl
Ju Young Kim, Min Kyu Park, Yong Ju Lee, Sun Huh, Ky Young Cho
Pediatric Infection and Vaccine.2018; 25(1): 54. CrossRef
Development of an immunodiagnosis method using recombinant PsCP for detection of Paragonimus skrjabini infection in human
Shasha Yu, Xilin Zhang, Wenbi Chen, Hong Zheng, Guoping Ai, Nan Ye, Ying Wang
Parasitology Research.2017; 116(1): 377. CrossRef
Molecular identification of the trematode Paragonimus in faecal samples from the wild cat Prionailurus bengalensis in the Da Krong Nature Reserve, Vietnam
P.N. Doanh, H.V. Hien, L.A. Tu, N. Nonaka, Y. Horii, Y. Nawa
Journal of Helminthology.2016; 90(6): 658. CrossRef
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
Parasitology.2016; 143(12): 1639. CrossRef
A tool for mass-screening of paragonimiasis: an enzyme-linked immunosorbent assay with urine samples
Xu Guang Qiu, Fukumi Nakamura-Uchiyama, Yukifumi Nawa, Makoto Itoh
Tropical Medicine and Health.2016;[Epub] CrossRef

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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

Citations to this article as recorded by

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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Paragonimiasis in the Abdominal Cavity and Subcutaneous Tissue: Report of 3 Cases: Chang Ho Lee, Jong Hun Kim, Woo Sung Moon, Min Ro Lee; Korean J Parasitol 2012;50(4):345-347.
Published online November 26, 2012; DOI: https://doi.org/10.3347/kjp.2012.50.4.345

Abstract
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Paragonimiasis is a parasitic disease caused by the lung fluke, Paragonimus spp. Lung flukes may be found in various organs, such as the brain, peritoneum, subcutaneous tissues, and retroperitoneum, other than the lungs. Abdominal paragonimiasis raises a considerable diagnostic challenge to clinicians, because it is uncommon and may be confused with other abdominopelvic inflammatory diseases, particularly peritoneal tuberculosis, and peritoneal carcinomatosis. Also, subcutaneous paragonimiasis does not easily bring up clinical suspicion, due to its rarity. We herein report 2 cases of abdominal paragonimiasis and 1 case of subcutaneous paragonimiasis in Korea.

Citations

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Survival and infectivity of Paragonimus westermani Metacercariae in soy sauce–marinated crayfish
Eun-Min Kim, Yan Jin, Sung-Tae Hong
Food and Waterborne Parasitology.2025; 40: e00277. CrossRef
Pulmonary, liver and cerebral paragonimiasis: An unusual clinical case in Colombia
Angel O. Donato-R., Jhon C. Donato-R.
Travel Medicine and Infectious Disease.2022; 46: 102253. CrossRef
Ectopic peritoneal paragonimiasis mimicking tuberculous peritonitis: A care report
Jung Woo Choi, Chang Min Lee, Seong Je Kim, Se In Hah, Ji Yoon Kwak, Hyun Chin Cho, Chang Yoon Ha, Woon Tae Jung, Ok Jae Lee
World Journal of Clinical Cases.2022; 10(16): 5359. CrossRef
Intraspinal Paragonimiasis in Children: MRI Findings and Suggestions for Pathogenesis
Y. Qin, J. Cai, W. Ji, X. Chen, L. Tian, S. Jun, L. Wang, X. He
American Journal of Neuroradiology.2019;[Epub] CrossRef
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
Inactivation of Paragonimus westermani metacercariae in soy sauce-marinated and frozen freshwater crabs
Tae Im Kim, Se-Ra Oh, Fuhong Dai, Hyun-Jong Yang, Sang-Do Ha, Sung-Jong Hong
Parasitology Research.2017; 116(3): 1003. CrossRef
Paragonimiasis in Children in Southwest China
Zongrong Gong, Ruixue Miao, Min Shu, Yu Zhu, Yang Wen, Qin Guo, Qiong Liao, Chaomin Wan
Medicine.2017; 96(25): e7265. CrossRef
Recent Incidence of Paragonimus westermani Metacercariae in Freshwater Crayfish, Cambaroides similis, from Two Enzootic Sites in Jeollanam-do, Korea
Jin-Ho Song, Fuhong Dai, Xuelian Bai, Tae-Im Kim, Hyun-Jong Yang, Tong-Soo Kim, Shin-Hyung Cho, Sung-Jong Hong
The Korean Journal of Parasitology.2017; 55(3): 347. 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
Hepatic paragonimiasis in a 15-month-old girl: a case report
Zongrong Gong, Zhicheng Xu, Chuanfen Lei, Chaomin Wan
BMC Pediatrics.2017;[Epub] CrossRef
Distinct MDCT imaging features to differential diagnosis of hepatic paragonimiasis and small hepatocellular carcinoma
Sheng Zhang, Si-Ming Xie, Yong-Hua Chen, Xu-Bao Liu, Gang Mai
Oncotarget.2017; 8(23): 37291. CrossRef
A Case of Intra-abdominal Paragonimiasis Mimicking Metastasis of Lung Cancer Diagnosed by Endoscopic Ultrasound-guided Fine Needle Aspiration
Cho Rong Oh, Mi-Jin Kim, Kwang Hyuck Lee
The Korean Journal of Gastroenterology.2015; 66(1): 41. CrossRef
Pancreatic paragonimiasis mimics pancreatic cystic-solid tumor – A case report
Xiaodong Yang, Mingqing Xu, Yang Wu, Bo Xiang
Pancreatology.2015; 15(5): 576. CrossRef
Cutaneous paragonimiasis due to triploid Paragonimus westermani presenting as a non-migratory subcutaneous nodule: a case report
Makoto Kodama, Mayumi Akaki, Hiroyuki Tanaka, Haruhiko Maruyama, Eiji Nagayasu, Tetsuhiro Yokouchi, Yasuji Arimura, Hiroaki Kataoka
Journal of Medical Case Reports.2014;[Epub] CrossRef
Clinical Update on Parasitic Diseases
Min Seo
Korean Journal of Medicine.2013; 85(5): 469. CrossRef
Paragonimiasis: A Pictorial Essay
Kyung Nyeo Jeon, Mi Jung Park, Kyungsoo Bae, Hae Young Choi, Ho Cheol Choi, Jae Boem Na, Dae Seob Choi, Ho Cheol Kim, In Seok Jang, Dong Chul Kim
Journal of the Korean Society of Radiology.2013; 69(5): 365. CrossRef

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A Paragonimiasis Patient with Allergic Reaction to Praziquantel and Resistance to Triclabendazole: Successful Treatment after Desensitization to Praziquantel: Sun Young Kyung, Yong Kyun Cho, Yu Jin Kim, Jeong-Woong Park, Sung Hwan Jeong, Jae-Ik Lee, Yon Mi Sung, Sang Pyo Lee; Korean J Parasitol 2011;49(1):73-77.
Published online March 18, 2011; DOI: https://doi.org/10.3347/kjp.2011.49.1.73

Abstract
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Paragonimiasis is an infectious disease caused by trematodes of the genus Paragonimus. This trematode can be treated successfully with praziquantel in more than 90% of the cases. Although praziquantel is generally well tolerated, anaphylactic reactions to this drug have been reported in a few cases. We report here a 46-year-old Korean female with paragonimiasis, presumed to be due to Paragonimus westermani, who displayed an allergic reaction to praziquantel and resistance to triclabendazole treatment. The patient was successfully treated with praziquantel following a rapid desensitization procedure. Desensitization to praziquantel could be considered when no alternative drugs are available.

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A Review on Paragonimiasis and its Differential Diagnosis Technique
Vekutolu Resuh, Avolu Kotso, Viswedenu Kera, Lipoksenla Walling, Ibasiewdor Mawlein, Wankupar Wankhar
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Anaphylactic reaction to praziquantel following schistosomiasis treatment
Géssica Almeida Vasconcelos, Bernardo Gratival Gouvea Costa, Ronald Alves dos Santos, Carolina Dourado de Faria, Fernando Antônio Ramos Schramm Neto, Yuri de Jesus Machado, Ane Caroline Casaes, Marcos Vinicius Lima de Oliveira, Thainá Rodrigues de Souza F
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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
PDF

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 Communication

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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Eun-Min Kim, Yan Jin, Sung-Tae Hong
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Inactivation of Paragonimus westermani metacercariae in soy sauce-marinated and frozen freshwater crabs
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Parasitology Research.2017; 116(3): 1003. CrossRef
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Jin-Ho Song, Fuhong Dai, Xuelian Bai, Tae-Im Kim, Hyun-Jong Yang, Tong-Soo Kim, Shin-Hyung Cho, Sung-Jong Hong
The Korean Journal of Parasitology.2017; 55(3): 347. CrossRef
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Case Report

Three Cases of Paragonimiasis in a Family: Byeong Seok Sohn, Yun-Jeong Bae, You Sook Cho, Hee-Bom Moon, Tae-Bum Kim; Korean J Parasitol 2009;47(3):281-285.
Published online August 28, 2009; DOI: https://doi.org/10.3347/kjp.2009.47.3.281

Abstract
PDF

Paragonimiasis typically results from the consumption of raw or improperly cooked crustacea, especially crabs and crayfish. Although previously endemic in Korea, the prevalence of this disease decreased in the early 1970s because of educational campaigns and fewer intermediate hosts as a result of ecological changes. Recently, we were presented with a family where all members were infected with Paragonimus after ingestion of Kejang (= drunken crab). The mother was hospitalized for general myalgia and weakness first, followed by the father, who was hospitalized for dyspnea 2 month later. After the parents were diagnosed with paragonimiasis, we recommended their daughter to visit our hospital for a checkup, because they all had eaten freshwater crabs soaked in soybean sauce. She complained of generalized myalgia, fever, and pleuritic pain, and was also diagnosed with paragonimiasis. Peripheral blood of the 3 patients revealed hypereosinophilia, and computed tomography (CT) scans of their chests showed pleural effusion. The results of antibody tests by ELISA were positive for paragonimiasis. We report here the case series of familial paragonimiasis in a modern urban city, rather than in a typical endemic area.

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Original Article

Indochinamon ou (Crustacea: Potamidae) as a New Second Intermediate Host for Paragonimus harinasutai in Luang Prabang Province, Lao PDR: Woon-Mok Sohn, Jae-Sook Ryu, Duk-Young Min, Hyun-Ouk Song, Han-Jong Rim, Youthanavanh Vonghachack, Daluny Bouakhasith, Virasack Banouvong; Korean J Parasitol 2009;47(1):25-29.
Published online March 12, 2009; DOI: https://doi.org/10.3347/kjp.2009.47.1.25

Abstract
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Paragonimus harinasutai metacercariae were found in a species of freshwater crab, Indochinamon ou, collected in a small stream of Namback District, Luang Prabang Province, Lao PDR. Adult flukes were recovered after experimental infection of the metacercariae to dogs. Metacercariae were round or slightly elliptical, 0.666 × 0.626 mm in average size, and had a thin cyst wall of about 20 ?m in thickness, a black excretory bladder, convoluted ceca, and some pinkish materials in the body. Adults were somewhat elongated, 95.2 × 36.5 mm in average size, covered with single-tipped tegumental spines, had a smaller oral sucker than the ventral sucker, a moderately branched ovary, and 5-6 lobulated testes. Eggs were ovoid and bilaterally symmetrical in shape, 79 × 45 ?m in average size, and had a uniformly thickened shell. By the present study, it has been confirmed that I. ou is a new second intermediate host for P. harinasutai.

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Considerable genetic diversity within Paragonimus heterotremus in Luang Prabang, northern Lao People's Democratic Republic
Alongkorn Nonthapa, Rutchanee Rodpai, Tongjit Thanchomnang, Patcharaporn Boonroumkaew, Lakkhana Sadaow, David Blair, Pewpan M. Intapan, Wanchai Maleewong, Virasack Banouvong, Sakhone Laymanivong, Oranuch Sanpool
Infection, Genetics and Evolution.2025; 128: 105718. CrossRef
Usefulness and limits of Ziehl-Neelsen staining to detect paragonimiasis in highly endemic tuberculosis areas
Kethmany Ratsavong, Fabrice Quet, Fulgence Nzabintwali, Jeoffray Diendéré, Jacques Sebert, Michel Strobel, Yves Buisson
Parasite Epidemiology and Control.2017; 2(1): 1. CrossRef
Morphological and molecular identification of a lung fluke, Paragonimus macrorchis (Trematoda, Paragonimidae), found in central Lao PDR and its molecular phylogenetic status in the genus Paragonimus
Oranuch Sanpool, Pewpan Maleewong Intapan, Tongjit Thanchomnang, Penchom Janwan, Sakhone Laymanivong, Hiromu Sugiyama, Wanchai Maleewong
Parasitology International.2015; 64(6): 513. CrossRef

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Brief Communications

Skin Test for Paragonimiasis among Schoolchildren and Villagers in Namback District, Luangprabang Province, Lao PDR: Hyun-Ouk Song, Duk-Young Min, Han-Jong Rim, Vonghachack Youthanavanh, Bouakhasith Daluny, Vongsouvan Sengdara, Banouvong Virasack, Phommasak Bounlay; Korean J Parasitol 2008;46(3):179-182.
Published online September 20, 2008; DOI: https://doi.org/10.3347/kjp.2008.46.3.179

Abstract
PDF

As a part of a broader effort to determine the status of Paragonimus species infection in Lao PDR, an epidemiological survey was conducted on villagers and schoolchildren in Namback District between 2003 and 2005. Among 308 villagers and 633 primary and secondary schoolchildren, 156 villagers and 92 children evidenced a positive reaction on a Paragonimus skin test. Only 4 schoolchildren out of 128 skin test-positive cases had Paragonimus sp. eggs in their sputum, all of which was collected on 1 day. Several types of crabs, which were identified as the second intermediate host of the Paragonimus species, were collected from markets and streams in a paragonimiasis endemic area for the inspection of metacercariae. Among the examined crabs, only "rock crabs" (Indochinamon ou) harbored Paragonimus sp. metacercariae, and it is speculated that the life cycle of Paragonimus sp. was maintained via rock crabs in Namback District, Lao PDR.

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Paragonimus and paragonimiasis in Asia: An update
Ayako Yoshida, Pham Ngoc Doanh, Haruhiko Maruyama
Acta Tropica.2019; 199: 105074. CrossRef
Usefulness and limits of Ziehl-Neelsen staining to detect paragonimiasis in highly endemic tuberculosis areas
Kethmany Ratsavong, Fabrice Quet, Fulgence Nzabintwali, Jeoffray Diendéré, Jacques Sebert, Michel Strobel, Yves Buisson
Parasite Epidemiology and Control.2017; 2(1): 1. CrossRef

7,927 View
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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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International Journal of Infectious Diseases.2008; 12(6): e49. CrossRef

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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
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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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Alessandra L. Morassutti, Carlos Graeff-Teixeira
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Yasuhito Sako, Kazuhiro Nakaya, Akira Ito
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Eosinophil and Tissue-invasive Parasitic Helminth
Myeong Heon Shin
Hanyang Medical Reviews.2010; 30(3): 238. CrossRef
Eosinophil-Mediated Tissue Inflammatory Responses in Helminth Infection
Myeong Heon Shin, Young Ah Lee, Duk-Young Min
The Korean Journal of Parasitology.2009; 47(Suppl): S125. CrossRef
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
The Korean Journal of Parasitology.2008; 46(2): 95. CrossRef
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Identification of immunodominant excretory–secretory cysteine proteases of adult Paragonimus westermani by proteome analysis
Eung‐Goo Lee, Byoung‐Kuk Na, Young‐An Bae, Seon‐Hee Kim, Eun‐Young Je, Jeong‐Won Ju, Shin‐Hyeong Cho, Tong‐Soo Kim, Shin‐Yong Kang, Seung‐Yull Cho, Yoon Kong
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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
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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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American Journal of Plant Sciences.2012; 03(12): 1820. CrossRef
PwRn1, a novel Ty3/gypsy-like retrotransposon of Paragonimus westermani: molecular characters and its differentially preserved mobile potential according to host chromosomal polyploidy
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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
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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

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Immunoelectron microscopic localization of partially purified antigens in adult Paragonimus iloktsuenensis: Ok-Ran Lee, Pyung-Rim Chung; Korean J Parasitol 2001;39(2):119-132.
Published online June 30, 2001; DOI: https://doi.org/10.3347/kjp.2001.39.2.119

Abstract
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An immunoelectron microscopy employing immunogold labeling method was performed to detect tissue origin of D1 fraction (D1A) among 5 antigenic protein fractions partially purified by DEAE-anion exchange chromatography from water-soluble crude antigen (PIWA) of adult Paragonimus iloktsuenensis. Immune reactions of adult worm tissues with rabbit serum immunoglobulin immunized with crude antigen (PI-Ig) and D1 antigen (D1-Ig), as well as rat serum immunoglobulin infected with P. iloktsuenensis were observed. D1A showed strong antigenicity in the intestinal epithelium of the worms during the early infection period of 2-4 weeks after infection. The vitellaria also showed stronger antigenicity than the other tissue sites in immune reaction of tissues against all immunoglobulins from 4 to 33 weeks after vitelline development. Therefore, it is suggested that D1A was mainly originated from the intestinal epithelial tissues before the development of vitelline gland of the parasites. Immuno-reactivity of two immunoglobulins (PI-Ig, D1-Ig) was significantly different in intestinal epithelial cytoplasmic protrusions (CP) and intestinal epithelial secretory granules (SG). In the experimental group with D1-Ig, gold particles were labeled significantly in CP than in SG when compared to the PI-Ig group. Thus, the major antigenic materials in D1 antigen having a strong antigenicity in the early infection period was considered to be originated from the intestinal epithelial tissue.

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