Advertisement

Intestinal Trematode Infections

  • Rafael ToledoEmail author
  • Maria Alvárez-Izquierdo
  • Carla Muñoz-Antoli
  • J. Guillermo Esteban
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1154)

Abstract

Intestinal trematodes are among the most common types of parasitic worms. About 76 species belonging to 14 families have been recorded infecting humans. Infection commonly occurs when humans eat raw or undercooked foods that contain the infective metacercariae. These parasites are diverse with regard to their morphology, geographical distribution, and life cycle, which make it difficult to study the parasitic diseases that they cause. Many of these intestinal trematodes have been considered as endemic parasites in the past. However, the geographical limits and the population at risk are currently expanding and changing in relation to factors such as growing international markets, improved transportation systems, new eating habits in developed countries and demographic changes. These factors make it necessary to better understand intestinal trematode infections. This chapter describes the main features of human intestinal trematodes in relation to their biology, epidemiology, host–parasite relationships, pathogenicity, clinical aspects, diagnosis, treatment, and control.

Keywords

Digenea Trematode infection Intestinal trematodesbiologyepidemiologyhost–parasite relationshipspathogenicitydiagnosistreatmentcontrol 

Notes

Acknowledgements

This work was supported supported by Ministerio de Economía y Competitividad (Madrid, Spain) (grant number: BFU2016-75639-P) and by Ministerio de Sanidad y Consumo (Madrid, Spain) (No. RD12/0018/0013, Red de Investigación Cooperativa en Enfermedades Tropicales—RICET, IV National Program of I+D+I 2008-2011, ISCIII—Subdirección General de Redes y Centros de Investigación Cooperativa and FEDER).

References

  1. Agger MK, Simonsen PE, Vennervald BJ (1993) The antibody response in serum, intestinal wall and intestinal lumen of NMRI mice infected with Echinostoma caproni. J Helminthol 67:169–178PubMedCrossRefGoogle Scholar
  2. Asada JI, Otagaki H, Morita M, Takeuchi T, Sakai Y, Kojishi T, Okahashi K (1962) A case report on the human infection with Plagiorchis muris Tanabe, 1922 in Japan. Jpn J Parasitol 11:512–516Google Scholar
  3. Ashour DS, Othman AA, Radi DA (2014) Insights into regulatory molecules of intestinal epithelial cell turnover during experimental infection by Heterophyes heterophyes. Exp Parasitol 143:48–54PubMedCrossRefGoogle Scholar
  4. Bandyopadhyay AK, Nandy A (1986) A preliminary observation on the prevalence of echinostomes in a tribal community near Calcutta. Ann Trop Med Parasitol 80:373–375PubMedCrossRefGoogle Scholar
  5. Bandyopadhyay AK, Manna B, Nandy A (1989) Human infection of Artyfechinostomum oraoni n. sp. (Paryphostominae: Echinostomatidae) in a tribal community, “Oraons” in West Bengal, India. Indian J Parasitol 13:191–196Google Scholar
  6. Beaver PC, Jung RC, Cupp EW (1984) Clinical parasitology, 9th edn. Lea and Febiger, PhiladelphiaGoogle Scholar
  7. Belizario VY, Geronilla GG, Anastacio MBM, de Leon WU, Suba-an AU, Sebastian AC, Bangs MJ (2007) Echinostoma malayanum infection, in the Philippines. Emerg Infect Dis 13:1130–1131PubMedCrossRefPubMedCentralGoogle Scholar
  8. Bhattacharjee HK, Yadav D, Bagga D (2009) Fasciolopsis presenting as intestinal perforation: a case report. Trop Gastroenterol 30:40–41PubMedGoogle Scholar
  9. Brunet LR, Joseph S, Dunne DW et al (2000) Immune responses during the acute stages of infection with the intestinal trematode Echinostoma caproni. Parasitology 120:565–571PubMedCrossRefGoogle Scholar
  10. Buckley JJC (1939) Observations on Gastrodiscoides hominis and Fasciolopsis buski in Assam. J Helminthol 17:1–12CrossRefGoogle Scholar
  11. Bunnag D, Radomyos P, Harinasuta T (1983) Field trial on the treatment of fasciolopsiasis with praziquantel. Southeast Asian J Trop Med Public Health 14:216–219PubMedPubMedCentralGoogle Scholar
  12. Butcher AR, Grove DI (2001) Description of the life-cycle stages of Brachylaima cribbi n. sp. (Digenea: Brachylaimidae) derived from eggs recovered from human faeces in Australia. Syst Parasitol 49:211–221PubMedCrossRefPubMedCentralGoogle Scholar
  13. Butcher AR, Talbot GA, Norton RE, Kirk MD, Cribb TH, Forsyth JR, Knight B, Cameron AS (1996) Locally acquired Brachylaima sp. (Digenea: Brachylaimidae) intestinal fluke infection in two South Australian infants. Med J Aust 164:475–478PubMedPubMedCentralGoogle Scholar
  14. Butcher AR, Parasuramar PS, Thompson CS, Grove DI (1998) First report of the isolation of an adult worm of the genus Brachylaima (Digenea: Brachylaimidae), from the gastrointestinal tract of a human. Int J Parasitol 28:607–610PubMedCrossRefPubMedCentralGoogle Scholar
  15. Butcher AR, Palethorpe HM, Grove DI (2002) Effects of sex and age on the susceptibility of C57BL/6J mice to infection with Brachylaima cribbi and the course of the infection in NOD SCID mice. Parasitol Res 88:668–674PubMedCrossRefPubMedCentralGoogle Scholar
  16. Butcher AR, Palethorpe HM, Grove DI (2003) Response to re-infection with Brachylaima cribbi in immunocompetent and immunodeficient mice. Parasitol Int 52:219–228PubMedCrossRefPubMedCentralGoogle Scholar
  17. Cao YH, Ma YM, Qiu F, Zhang XQ (2015) Rare cause of appendicitis: mechanical obstruction due to Fasciolopsis buski infestation. World J Gastroenterol 21:3146–3149PubMedPubMedCentralCrossRefGoogle Scholar
  18. Carney WP (1991) Echinostomiasis—a snail-borne intestinal disease. Southeast Asian J Trop Med Public Health 22:206–211PubMedPubMedCentralGoogle Scholar
  19. Carney WP, Sudomo M, Purnomo A (1980) Echinostomiasis: a disease that disappeared. Trop Geogr Med 32:101–105PubMedPubMedCentralGoogle Scholar
  20. Chai JY (2007) Intestinal flukes. In: Murrell KD, Fried B (eds) Food-borne parasitic zoonoses: fish and plant-borne parasites, world class parasites, vol 1. Springer, New York, pp 53–115CrossRefGoogle Scholar
  21. Chai JY (2009) Echinostomes in humans. In: Fried B, Toledo R (eds) The biology of Echinostomes. From the molecule to the community. Springer, New York, pp 147–183Google Scholar
  22. Chai JY, Lee SH (1991) Intestinal trematodes infecting humans in Korea. Southeast Asian J Trop Med Public Health 22:163–170PubMedPubMedCentralGoogle Scholar
  23. Chai JY, Lee SH (2002) Food-borne intestinal trematode infections in the Republic of Korea. Parasitol Int 51:129–154PubMedCrossRefPubMedCentralGoogle Scholar
  24. Chai JY, Seo BS, Lee SH, Hong SJ, Sohn WM (1986) Human infections by Heterophyes heterophyes and H. dispar imported from Saudi Arabia. Korean J Parasitol 24:82–88CrossRefGoogle Scholar
  25. Chai JY, Huh S, Yu JR (1993) An epidemiological study of metagonimiasis along the upper reaches of the Namhau River. Korean J Parasitol 31:99–108PubMedCrossRefPubMedCentralGoogle Scholar
  26. Chai JY, Hong ST, Lee SH, Lee GC, Min YI (1994) A case of echinostomiasis with ulcerative lesions in the duodenum. Korean J Parasitol 32:201–204PubMedCrossRefPubMedCentralGoogle Scholar
  27. Chai JY, Kim IM, Seo M, Guk SM, Kim JL, Sohn WM, Lee SH (1997) A new focus of Heterophyes nocens, Pygidiopsis summa, and other intestinal flukes in a coastal area of Muan-gun, Chollanam-do. Korean J Parasitol 35:233–238PubMedCrossRefPubMedCentralGoogle Scholar
  28. Chai JY, Kim TK, Cho WH, Seo M, Kook J, Guk SM, Lee SH (1998) Intestinal mastocytosis and goblet cell hyperplasia in BALB/c and C3H mice infected with Neodiplostomum seoulense. Korean J Parasitol 36:109–119PubMedCrossRefPubMedCentralGoogle Scholar
  29. Chai JY, Chung WJ, Kook J, Seo M, Park YK, Guk SM, Choi MH, Lee SH (1999) Growth and development of Gymnophalloides seoi in immunocompetent and immunosupressed C3H/HeN mice. Korean J Parasitol 37:21–26PubMedPubMedCentralCrossRefGoogle Scholar
  30. Chai JY, Lee HS, Hong SJ, Yoo JH, Guk SM, Seo M, Choi MH, Lee SH (2001) Intestinal histopathology and in situ postures of Gymnophalloides seoi in experimentally infected mice. Korean J Parasitol 39:31–41PubMedPubMedCentralCrossRefGoogle Scholar
  31. Chai JY, Choi MH, Yu JR, Lee SH (2003) Gymnophalloides seoi, a new human intestinal trematode. Trends Parasitol 19:109–112PubMedCrossRefPubMedCentralGoogle Scholar
  32. Chai JY, Park JH, Han ET, Shin EH, Kim JL, Guk SM, Hong KS, Lee SH, Rim HJ (2004) Prevalence of Heterophyes nocens and Pygydiopsis summa infections among residents in Western and Southern coastal islands of the Republic of Korea. Am J Trop Med Hyg 71:617–622PubMedCrossRefPubMedCentralGoogle Scholar
  33. Chai JY, Shin EH, Lee SH, Rim HJ (2009a) Foodborne intestinal flukes in Southeast Asia. Korean J Parasitol 47:S69–S102PubMedPubMedCentralCrossRefGoogle Scholar
  34. Chai JY, Han ET, Shin EH, Sohn WM, Yong TS, Eom KS, Min DY, Um JY, Park MS, Hoang EH, Phommasack B, Insisiengmay B, Lee SH, Rim HJ (2009b) High prevalence of Haplorchis taichui, Phaneropsolus molenkampi, and other helminth infections among people in Khammouane province, Lao PDR. Korean J Parasitol 47:243–247PubMedPubMedCentralCrossRefGoogle Scholar
  35. Chai JY, Sohn WM, Yong TS, Eom KS, Min DY, Hoang EH, Phammasack B, Insisiengmay B, Rim HJ (2012) Echinostome flukes recovered from humans in Khammouane Province, Lao PDR. Korean J Parasitol 50:269–272PubMedPubMedCentralCrossRefGoogle Scholar
  36. Chai JY, Sohn WM, Yong TS, Eom KS, Min DY, Lee MY, Lim H, Insisiengmay B, Phommasack B, Rim HJ (2013) Centrocestus formosanus (Heterophyidae): human infections and the infection source in Lao PDR. J Parasitol 99:531–536PubMedCrossRefPubMedCentralGoogle Scholar
  37. Chai JY, Sohn WM, Cho J, Eom KS, Yong TS, Min DY, Hoang EH, Phommasack B, Insisiengmay B, Rim HJ (2018) Echinostoma ilocanum infection in two residents of Savannakhet Province, Lao PDR. Korean J Parasitol 56:75–79PubMedPubMedCentralCrossRefGoogle Scholar
  38. Chang YD, Sohn WM, Ryu JH, Kang SY, Hong SJ (2005) A human infection of Echinostoma hortense in duodenal bulb diagnosed by endoscopy. Korean J Parasitol 43:57–60PubMedPubMedCentralCrossRefGoogle Scholar
  39. Chen CE, Cai GD (1985) Morphological testimony: demonstration of a case of human infestation with Cotylurus japonicus Ishii, 1932 (Trematoda, Strigeidae). Bull Hum Med 10:31–34Google Scholar
  40. Chen XQ, Feng GX, Qian ZF (1993) Survey on infection due to Echinostoma hortense in Liaoning Province. Chin J Parasitol Parasit Dis 11:226Google Scholar
  41. Cheng YZ, Lin JX, Fang YY, Lin AQ, Chen BJ, Zhunag HJ (1992) Discovery of human infection with Echinostoma angustitestis. Chin J Zoonoses 8:7–8Google Scholar
  42. Chi JG, Kim CW, Kim JR, Hong ST, Lee SH (1988) Intestinal pathology in human metagonimiasis with ultrastructural observations of parasites. J Korean Med Sci 3:171–177PubMedPubMedCentralCrossRefGoogle Scholar
  43. Chieffi PP, Gorla MC, Torres DM, Dias RM, Mangini AC, Monteiro AV, Woiciechovski E (1992) Human infection by Phagicola sp. (Trematoda, Heterophyidae) in the municipality of Registro, São Paulo State, Brazil. J Trop Med Hyg 95:346–348PubMedPubMedCentralGoogle Scholar
  44. Cho SY, Kim SI, Kang SY (1987) Specific IgG responses in experimental cat metagonimiasis. Korean J Parasitol 25:149–153CrossRefGoogle Scholar
  45. Cho CM, Tak WY, Kweon YO, Kim SK, Choi YH, Kong HH, Chung DI (2003) A human case of Echinostoma hortense (Trematoda: Echinostomatidae) infection diagnosed by gastroduodenal endoscopy in Korea. Korean J Parasitol 41:117–120PubMedPubMedCentralCrossRefGoogle Scholar
  46. Cho YK, Ryang YS, Kim IS, Park SK, Im JA, Lee KJ (2007) Differential immune profiles following experimental Echinostoma hortense infection in BALB/c and C3H/HeN mice. Parasitol Res 100:1053–1061PubMedCrossRefPubMedCentralGoogle Scholar
  47. Cho SH, Cho PY, Lee DM, Kim TS, Kim IS, Hwang EJ, Na BK, Sohn WM (2010) Epidemiological survey on the infection of intestinal flukes in residents of Muan-gun, Jeollanam-do, the Republic of Korea. Korean J Parasitol 48:133–138PubMedPubMedCentralCrossRefGoogle Scholar
  48. Chung PR, Jung Y, Kim DS (1996) Segmentina (Polypylis) hemisphaerula (Gastropoda: Planorbidae): a new molluscan intermediate host of a human intestinal fluke Neodiplostomum seoulensis (Trematoda: Diplostomatidae) in Korea. J Parasitol 82:336–338PubMedCrossRefPubMedCentralGoogle Scholar
  49. Chung PR, Jung Y, Park YK, Hwang MG (2002) Host specificity of Austropeplea ollula (Gastropoda: Lymnaeidae) to miracidial infection with a human intestinal fluke Neodiplostomum seoulense (Trematoda: Diplostomatidae) in Korea. J Parasitol 88:630–631PubMedCrossRefPubMedCentralGoogle Scholar
  50. Chung OS, Lee HJ, Kim YM, Sohn WM, Kwak SJ, Seo M (2011) First report of human infection with Gynaecotyla squatarolae and first Korean record of Haplorchis pumilio in a patient. Parasitol Int 60:227–229PubMedCrossRefPubMedCentralGoogle Scholar
  51. Chunge RN, Chunge CN (2017) Infection with Echinostoma sp. in a group of travellers to Lake Tanganyika, Tanzania, in January 2017. J Travel Med 24(5): 1–3Google Scholar
  52. Clarke MD, Carney WP, Cross JH, Hadidjaja P, Oemijati S, Joesoef A (1974) Schistosomiasis and other human parasitoses of Lake Lindu in Central Suwalesi (Celebes), Indonesia. Am J Trop Med Hyg 23:385–392PubMedCrossRefGoogle Scholar
  53. Cortés A, Sotillo J, Muñoz-Antoli C, Fried B, Esteban JG, Toledo R (2014) Intestinal IFN-γ production is associated with protection from clinical signs, but not with elimination of worms, in Echinostoma caproni infected-mice. Parasitol Res 113:2037–2045PubMedCrossRefGoogle Scholar
  54. Cortés A, Sotillo J, Muñoz-Antoli C, Fried B, Esteban JG, Toledo R (2015a) Altered protein expression in the ileum of mice associated with the development of chronic infections with Echinostoma caproni (Trematoda). PLoS Negl Trop Dis 9:e0004082PubMedPubMedCentralCrossRefGoogle Scholar
  55. Cortés A, Muñoz-Antoli C, Martín-Grau C, Esteban JG, Grencis RK, Toledo R (2015b) Differential alterations in the small intestine epithelial cell turnover during acute and chronic infection with Echinostoma caproni (Trematoda). Parasit Vectors 8:334PubMedPubMedCentralCrossRefGoogle Scholar
  56. Cortés A, Muñoz-Antoli C, Sotillo J, Fried B, Esteban JG, Toledo R (2015c) Echinostoma caproni (Trematoda): differential in vivo mucin expression and glycosylation in high- and low-compatible hosts. Parasite Immunol 37:32–42PubMedCrossRefGoogle Scholar
  57. Cortés A, Sotillo J, Muñoz-Antolí C, Trelis M, Esteban JG, Toledo R (2016) Definitive host influences the proteomic profile of excretory/secretory products of the trematode Echinostoma caproni. Parasit Vectors 9:185PubMedPubMedCentralCrossRefGoogle Scholar
  58. Cortés A, Sotillo J, Muñoz-Antolí C, Molina-Durán J, Esteban JG, Toledo R (2017a) Antibody trapping: a novel mechanism of parasite immune evasion by the trematode Echinostoma caproni. PLoS Negl Trop Dis 11:e0005773PubMedPubMedCentralCrossRefGoogle Scholar
  59. Cortés A, García-Ferrús M, Sotillo J, Esteban JG, Toledo R, Muñoz-Antolí C (2017b) Effects of dietary intake of garlic on intestinal trematodes. Parasitol Res 116:2119–2129PubMedCrossRefGoogle Scholar
  60. Cortés A, Muñoz-Antolí C, Álvarez-Izquierdo M, Sotillo J, Esteban JG, Toledo R (2018) Adaptation of the secretome of Echinostoma caproni may contribute to parasite survival in a Th1 milieu. Parasitol Res 117:947–957PubMedCrossRefGoogle Scholar
  61. Cremonte F, Pina S, Gilardoni C, Rodrigues P, Chai JY, Ituarte C (2013) A new species of gymnophallid (Digenea) and an amended diagnosis of the genus Gymnophalloides Fujita, 1925. J Parasitol 99:85–92PubMedCrossRefGoogle Scholar
  62. Cribb TH, Bray RA, Olson PD, Littlewood DT (2003) Life cycle evolution in the digenea: a new perspective from phylogeny. Adv Parasitol 54:197–254PubMedCrossRefGoogle Scholar
  63. Cross JH, Clarke MD, Cole WC (1976) Parasitic infection in humans in West Kalimantan (Borneo) Indonesia. Trop Geogr Med 28:121–130PubMedGoogle Scholar
  64. De NV, Le TH (2011) Human infections of fish-borne trematodes in Vietnam: prevalence and molecular specific identification at an endemic commune in Nam Dinh province. Exp Parasitol 129:355–361PubMedCrossRefPubMedCentralGoogle Scholar
  65. DeGirolami PC, Kimber J (1983) Intestinal parasites among Southeast Asian refugees in Massachusetts. Am J Clin Pathol 79:502–504PubMedCrossRefGoogle Scholar
  66. Ditrich O, Kopacek P, Giboda M, Gutvirth J, Scholz T (1991) Serological differentiation of human small fluke infections using Opisthorchis viverrini and Haplorchis taichui antigens. Southeast Asian J Trop Med Public Health 22:174–178PubMedPubMedCentralGoogle Scholar
  67. D’Souza PE, Jagannath MS, Prasanna KM (2001) A note on the occurrence of Fasciolopsis buski in pigs. Cheiron 30:178–179Google Scholar
  68. Eastburn RL, Fritsche TR, Terhune CA (1987) Human intestinal infection with Nanophyetus salminocola from salmonoid fishes. Am J Trop Med Hyg 36:586–591PubMedCrossRefPubMedCentralGoogle Scholar
  69. Eduardo SL (1991) Food-borne zoonoses in the Philippines. Southeast Asian J Trop Med Public Health 22:16–22PubMedGoogle Scholar
  70. El-Ganayni GA, Youssef ME, Handousa AE, Bou-Zakham AA, Hegazi MM (1989) Serum and intestinal immunoglobulins in heterophyiasis. J Egypt Soc Parasitol 19:219–223PubMedGoogle Scholar
  71. Eom KS, Son SY, Lee JS, Rim HJ (1985) Heterophyid trematodes (Heterophyopsis continua, Pygidiopsis summa and Heterophyes heterophyes nocens) from domestic cats in Korea. Korean J Parasitol 23:197–202CrossRefGoogle Scholar
  72. Esteban JG, Muñoz-Antoli C (2009) Echinostomes: systematics and life cycles. In: Fried B, Toledo R (eds) The biology of Echinostomes. From the molecule to the community. Springer, New York, pp 1–34Google Scholar
  73. Fathy FM (2011) Anthelmintic effect of artesunate in experimental heterophyiid infection. J Egypt Soc Parasitol 41:469–483PubMedGoogle Scholar
  74. Ferreira JFS, Peaden P, Keiser J (2011) In vitro trematocidal effects of crude alcoholic extracts of Artemisia annua, A. absinthium, Asimina triloba and Fumaria officinalis. Parasitol Res 109:1585–1582PubMedCrossRefGoogle Scholar
  75. Fried B, Toledo R (2004) Criteria for species determination in the “revolutum” group of Echinostoma. J Parasitol 90:917PubMedCrossRefGoogle Scholar
  76. Fried B, Graczyk TK, Tamang L (2004) Food-borne intestinal trematodiases in humans. Parasitol Res 93:159–170PubMedCrossRefPubMedCentralGoogle Scholar
  77. Fujino T, Fried B (1993) Expulsion of Echinostoma trivolvis (Cort, 1914) Kanev, 1985 and retention of E. caproni Richard, 1964 (Trematoda, Echinostomatidae) in C3H mice: pathological, ultrastructural, and cytochemical effects on the host intestine. Parasitol Res 79:286–292PubMedCrossRefGoogle Scholar
  78. Fujino T, Fried B (1996) The expulsion of Echinostoma trivolvis from C3H mice: differences in glycoconjugates in mouse versus hamster small intestinal mucosa during infection. J Helminthol 70:115–121PubMedCrossRefGoogle Scholar
  79. Fujino T, Fried B, Tada I (1993) The expulsion of Echinostoma trivolvis: worm kinetics and intestinal cytopathology in conventional and congenitally athymic BALB/c mice. Parasitology 106:297–304PubMedCrossRefGoogle Scholar
  80. Fujino T, Fried B, Ichikawa H, Tada I (1996a) Rapid expulsion of the intestinal trematodes Echinostoma trivolvis and E. caproni from C3H mice by trapping with increased goblet cell mucins. Int J Parasitol 26:319–324PubMedCrossRefGoogle Scholar
  81. Fujino T, Ichikawa H, Fried B, Fukuda K (1996b) The expulsion of Echinostoma trivolvis: suppressive effects of dexamethasone on goblet cell hyperplasia and worm rejection in C3H/HeN mice. Parasite 3:283–289PubMedCrossRefGoogle Scholar
  82. Fürst T, Keiser J, Utzinger J (2012a) Global burden of human food-borne trematodiasis: a systematic review and meta-analysis. Lancet Infect Dis 12:210–221PubMedCrossRefPubMedCentralGoogle Scholar
  83. Fürst T, Sayasone S, Odermatt P, Keiser J, Utzinger J (2012b) Manifestations, diagnosis, and management of foodborne trematodiasis. Br Med J 26:e4093CrossRefGoogle Scholar
  84. Gibson DI, Bray RA (1994) The evolutionary expansion and host-parasite relationship of the Digenea. Int J Parasitol 24:1213–1226PubMedCrossRefGoogle Scholar
  85. Gilman RH, Mondal G, Maskud M, Alam K, Rutherford E, Gilman JB, Khan MU (1982) Endemic focus of Fasciolopsis buski in Bangladesh. Am J Trop Med Hyg 31:796–802PubMedCrossRefGoogle Scholar
  86. Graczyk TK, Fried B (1994) ELISA method for detecting anti-Echinostoma caproni (Trematoda: Echinostomatidae) immunoglobulins in experimentally infected ICR mice. J Parasitol 80:544–549PubMedCrossRefGoogle Scholar
  87. Graczyk TK, Fried B (1995) An enzyme-linked immunosorbent assay for detecting anti-Echinostoma trivolvis (Trematoda) IgG in experimentally infected ICR mice. Cross-reactivity with E. caproni. Parasitol Res 81:710–712PubMedCrossRefGoogle Scholar
  88. Graczyk TK, Fried B (1998) Echinostomiasis: a common but forgotten food-borne disease. Am J Trop Med Hyg 58:501–504PubMedCrossRefGoogle Scholar
  89. Greenberg RM (2005) Are Ca2+ channels targets of praziquantel action? Int J Parasitol 35:1–9PubMedCrossRefGoogle Scholar
  90. Guk SM, Park JH, Shin EH, Kim JL, Lin A, Chai JY (2006) Prevalence of Gymnophalloides seoi infection in coastal villages of Haenamgun and Yeongam-gun, Republic of Korea. Korean J Parasitol 44:1–5PubMedPubMedCentralCrossRefGoogle Scholar
  91. Guk SM, Lee JH, Kim HJ, Kim WH, Shin EH, Chai JY (2009) CD4+ T-cell-dependent goblet cell proliferation and expulsion of Gymnophalloides seoi from the intestine of C57BL/6 mice. J Parasitol 95:581–590PubMedCrossRefPubMedCentralGoogle Scholar
  92. Han ET, Chen JH, Chai JY (2008) Antibody responses in sera of different mouse strains experimentally infected with Neodiplostomum seoulense. Korean J Parasitol 46:279–283PubMedPubMedCentralCrossRefGoogle Scholar
  93. Haseeb MA, Eveland LK (2000) Human echinostomiasis: mechanisms of pathogenesis and host resistance. In: Fried B, Graczyk TK (eds) Echinostomes as experimental models for biological research. Kluwer Academic Publishers, Dordrecht, pp 83–98CrossRefGoogle Scholar
  94. Hirazawa I (1928) On Echinochasmus perfoliatus (Ratz) found in man. Tokyo Iji Shinshi 2577:1328–1334Google Scholar
  95. Hong ST, Hong SJ, Lee SH, Seo BS, Chi JG (1982) Studies on intestinal trematodes in Korea: VI. On the metacercaria and the second intermediate host of Fibricola seoulensis. Korean J Parasitol 20:101–111CrossRefGoogle Scholar
  96. Hong SJ, Lee SH, Seo BS, Hong ST, Chai JY (1983) Studies on intestinal trematodes in Korea: IX. Recovery rate and development of Fibricola seoulensis in experimental animals. Korean J Parasitol 21:224–233CrossRefGoogle Scholar
  97. Hong ST, Chai JY, Lee SH (1984a) Ten human cases of Fibricola seoulensis infection and mixed one with Stellantchasmus and Metagonimus. Korean J Parasitol 24:95–97CrossRefGoogle Scholar
  98. Hong ST, Cho TK, Hong SJ, Chai JY, Lee SH, Seo BS (1984b) Fifteen human cases of Fibricola seoulensis infection in Korea. Korean J Parasitol 22:61–65CrossRefGoogle Scholar
  99. Hong SJ, Woo HC, Chai JY (1996) A human case of Plagiorchis muris (Tanabe, 1922: Digenea) infection in the Republic of Korea: freshwater fish as a possible source of infection. J Parasitol 82:647–649PubMedCrossRefPubMedCentralGoogle Scholar
  100. Huffman JE, Iglesias D, Fried B (1988) Echinostoma revolutum: pathology of extraintestinal infection in the golden hamster. Int J Parasitol 18:873–874PubMedCrossRefPubMedCentralGoogle Scholar
  101. Huh S, Hong ST (1993) Transmission electron microscopic findings of the tribocytic organ of Fibricola seoulensis. Korean J Parasitol 31:315–320PubMedCrossRefPubMedCentralGoogle Scholar
  102. Huh S, Chai JY, Hong ST, Lee SH (1988) Clinical and histopathological findings in mice heavily infected with Fibricola seoulensis. Korean J Parasitol 26:45–53CrossRefGoogle Scholar
  103. Huh S, Lee SH, Seo BS (1990) Histochemical findings of the tribocytic organ and tegument of Fibricola seoulensis. Korean J Parasitol 28:155–160CrossRefGoogle Scholar
  104. Jaroonvesama N, Charoenlarp K, Areekul S (1986) Intestinal absorption studies in Fasciolopsis buski infection. Southeast Asian J Trop Med Public Health 17:582–586PubMedPubMedCentralGoogle Scholar
  105. Jueco NL, Monzon RB (1984) Cathaemacia cabrerai sp. n. (Trematoda: Cathaemaciidae) a new oarqasite of man in the Philippines. Southeast Asian J Trop Med Public Health 15:427–429PubMedPubMedCentralGoogle Scholar
  106. Jung WT, Lee KJ, Kim HJ, Kim TH, Na BK, Sohn WM (2014) A case of Echinostoma cinetorchis (Trematoda: Echinostomatidae) infection diagnosed by colonoscopy. Korean J Parasitol 52:287–290PubMedPubMedCentralCrossRefGoogle Scholar
  107. Kaewkes S, Elkins DB, Haswell-Elkins MR, Sithithaworn P (1991) Phaneropsolus spinicirrus n. sp. (Digenea: Lecithodendriidae), a human parasite in Thailand. J Parasitol 77:514–516PubMedCrossRefPubMedCentralGoogle Scholar
  108. Kawahara S, Yamamoto E (1933) Human cases of Echinostoma cinetorchis. Tokyo Iji Shinshi 2840:1794–1796Google Scholar
  109. Keiser J, Utzinger J (2004) Chemotherapy for major food-borne trematodes: a review. Expert Opin Pharmacother 5:1711–1726PubMedCrossRefPubMedCentralGoogle Scholar
  110. Keiser J, Utzinger J (2009) Food-borne trematodiases. Clin Microbiol Rev 22:466–483PubMedPubMedCentralCrossRefGoogle Scholar
  111. Keiser J, Utzinger J (2010) The drugs we have and the drugs we need against major helminth infections. Adv Parasitol 73:197–230PubMedCrossRefPubMedCentralGoogle Scholar
  112. Keiser J, Brun R, Fried B, Utzinger J (2006a) Trematocidal activity of praziquantel and artemisinin derivatives: in vitro and in vivo investigations on adult Echinostoma caproni. Antimicrob Agents Chemother 50:803–805PubMedPubMedCentralCrossRefGoogle Scholar
  113. Keiser J, Utzinger J, Tanner M, Dong Y, Vennerstrom JL (2006b) The synthetic peroxide OZ78 is effective against Echinostoma caproni and Fasciola hepatica. J Antimicrob Chemother 58:1193–1197PubMedCrossRefPubMedCentralGoogle Scholar
  114. Kim I, Im JA, Lee KJ, Ryang YS (2000) Mucosal mast cell responses in the small intestine of rats infected with Echinostoma hortense. Korean J Parasitol 38:139–143PubMedPubMedCentralCrossRefGoogle Scholar
  115. Kim TY, Han KY, Shin EH, Chai JY (2008) Antigenic properties of cystatin-binding cysteine proteinases from Neodiplostomum seoulense. J Parasitol 94:654–658PubMedCrossRefPubMedCentralGoogle Scholar
  116. Kino H, Suzuki Y, Oishi H, Suzuki S, Yamagiwa S, Ishiguro M (2006) Geographical distribution of Metagonimus yokogawai, and M. miyatai in Shizuoka Prefecture, Japan, and their site preferences in the sweetfish, Plecoglossus altivelis, and hamsters. Parasitol Int 55:201–206PubMedCrossRefPubMedCentralGoogle Scholar
  117. Kook J, Nawa Y, Le SH, Chai JY (1998) Pathogenicity and lethality of a minute intestinal fluke, Neodiplostomum seoulense, to various strains of mice. Korean J Parasitol 84:1178–1183CrossRefGoogle Scholar
  118. Kostadinova A (2005) Family Echinostomatidae Looss, 1899. In: Gibson DI, Jones A, Bray RA (eds) Keys to the Trematoda, vol 2. CABI Publishing, Wallingford, pp 9–64CrossRefGoogle Scholar
  119. Kostadinova A, Gibson DI (2000) The systematics of the Echinostomes. In: Fried B, Graczyk TK (eds) Echinostomes as experimental models for biological research. Kluwer Academic Publishers, Dordrecht, pp 31–57CrossRefGoogle Scholar
  120. Kusharyono C, Sukartinah S (1991) The current status of foodborne parasitic zoonoses in Indonesia. Southeast Asian J Trop Med Public Health 22:8–10PubMedPubMedCentralGoogle Scholar
  121. Lee JB, Chi JG, Lee SK, Cho SY (1981) Study on the pathology of metagonimiasis in experimentally infected cat intestine. Korean J Parasitol 19:109–129CrossRefGoogle Scholar
  122. Lee SH, Yoo BH, Hong ST, Chai JY, Seo BS, Chi JG (1985) A histopathological study on the intestine of mice and rats experimentally infected by Fibricola seoulensis. Korean J Parasitol 23:58–72CrossRefGoogle Scholar
  123. Lee SK, Chung NS, Ko IH, Ko HI, Chai JY (1986) Two cases of natural human infection by Echinostoma hortense. Kisaengchunghak Chapchi 24:77–81PubMedPubMedCentralGoogle Scholar
  124. Lee SK, Chung NS, Ko IH (1988) An epidemiological survey of Echinostoma hortense infection in Chongsong-gun, Kyongbuk Province. Korean J Parasitol 26:199–206CrossRefGoogle Scholar
  125. Lee SH, Chai JY, Hong ST (1993a) Gymnophalloides seoi n. sp. (Digenea: Gymnophallidae), the first report of human infection by a gymnophallid. Korean J Parasitol 79:677–680CrossRefGoogle Scholar
  126. Lee SC, Chung YB, Kong Y, Kang SY, Cho SY (1993b) Antigenic protein fractions of Metagonimus yokogawai reacting with patient sera. Korean J Parasitol 31:43–48PubMedCrossRefPubMedCentralGoogle Scholar
  127. Lee SH, Chai JY, Seo M, Choi MH, Kim DC, Lee SK (1995) Two cases of Gymnophalloides seoi infection accompanied by diabetes mellitus. Korean J Parasitol 33:61–64PubMedCrossRefPubMedCentralGoogle Scholar
  128. Lee SH, Sohn WM, Hong SJ, Huh S, Seo M, Choi MH, Chai JY (1996) A nationwide survey of naturally produced oysters for infection with Gymnophalloides seoi metacercariae. Korean J Parasitol 34:107–112PubMedCrossRefPubMedCentralGoogle Scholar
  129. Lee JC, Kong Y, Lee SU, Huh S (1997a) Localization of worm antigen in Neodiplostomum seoulense by immuno-electronmicroscopy. Korean J Parasitol 35:95–104PubMedCrossRefPubMedCentralGoogle Scholar
  130. Lee SH, Park SK, Seo M, Guk SM, Choi MH, Chai JY (1997b) Susceptibility of various species of animals and strains of mice to Gymnophalloides seoi infection and the effects of immunosuppression in C3H/HeN mice. J Parasitol 83:883–886PubMedCrossRefPubMedCentralGoogle Scholar
  131. Lee JJ, Kim HJ, Kim MJ, Yi Lee JW, Jung BK, Lee JY, Shin EH, Kim JL, Chai JY (2008) Decrease of Metagonimus yokogawai endemicity along the Tamjin River basin. Korean J Parasitol 46:289–291PubMedPubMedCentralCrossRefGoogle Scholar
  132. Lee KJ, Jin D, Chang BS, Teng YC, Kim DH (2009) The immunological effects of electrolyzed reduced water on the Echinostoma hortense infection in C57BL/6 mice. Biol Pharm Bull 32:456–462PubMedCrossRefPubMedCentralGoogle Scholar
  133. Lee KD, Guk SM, Chai JY (2010) Toll-like receptor 2 and Muc2 expression on human intestinal epithelial cells by Gymnophalloides seoi adult antigen. J Parasitol 96:58–66PubMedCrossRefPubMedCentralGoogle Scholar
  134. Lee JJ, Jung BK, Lim H, Lee MY, Choi SY, Shin EH, Chai JY (2012) Comparative morphology of minute intestinal fluke eggs that can occur in human stools in the Republic of Korea. Korean J Parasitol 50:207–213PubMedPubMedCentralCrossRefGoogle Scholar
  135. Lee JJ, Kim D, Pyo KH, Kim MK, Kim HJ, Chai JY, Shin EH (2013) STAT6 expression and IL-13 production in association with goblet cell hyperplasia and worm expulsion of Gymnophalloides seoi from C57BL/6 mice. Korean J Parasitol 51:589–594PubMedPubMedCentralCrossRefGoogle Scholar
  136. Lee SH, Jung BK, Park JH, Shin EH, Chai JY (2014) Increased intestinal epithelial cell turnover and intestinal motility in Gymnophalloides seoi-infected C57BL/6 mice. Korean J Parasitol 52:273–280PubMedPubMedCentralCrossRefGoogle Scholar
  137. Liang C, Ke XL (1988) Echinochasmus jiufoensis sp. nov., a human parasite from Guangzhou (Trematoda: Echinostomatidae). Acta Zootaxa Sin 13:4–8Google Scholar
  138. Lu SC (1982) Echinostomiasis in Taiwan. Int J Zoonoses 9:33–38PubMedPubMedCentralGoogle Scholar
  139. Mabus J, Huffman JE, Fried B (1988) Humoral and cellular response to infection with Echinostoma revolutum in the golden hamster, Mesocricetus auratus. J Helminthol 62:127–132PubMedCrossRefPubMedCentralGoogle Scholar
  140. Mahanta J, Narain K, Srivastava VK (1995) Heterophyid eggs in human stool samples in Assam: first report for India. J Commun Dis 27:142–145PubMedPubMedCentralGoogle Scholar
  141. Majima M (1927) On Echinostoma macrorchis found in man. Kumamoto Igakkai Zasshi 2252:2260Google Scholar
  142. Manning GS, Brockelman WY, Yiyant V (1971) An analysis of the prevalence of Fasciolopsis buski in central Thailand using catalyitic models. Am J Epidemiol 93:354–360PubMedCrossRefPubMedCentralGoogle Scholar
  143. Martínez-Alonso JC, Armentia A, Vega JM, Callejo A, Gómez A (1999) Anaphylactic reaction concurrent with Heterophyes heterophyes infestation. Rev Esp Alergol Immunol Clín 14:37–39Google Scholar
  144. Marty AM, Andersen EM (2000) Fasciolopsiasis and other intestinal trematodiasis. In: Meyers WM, Neafie RC, Marty A, Wear DJ (eds) Pathology of infectious diseases, vol I. Helminthiases. Armed Forces Institute of Pathology, American Registry of Pathology, Washington, DCGoogle Scholar
  145. Mas-Coma S, Bargues MD, Valero MA (2005) Fascioliasis and other plant-borne trematode zoonoses. Int J Parasitol 35:1255–1278PubMedCrossRefPubMedCentralGoogle Scholar
  146. Mas-Coma S, Bargues MD, Valero MA (2006) Gastrodiscoidiasis, a plant-borne zoonotic disease caused by the intestinal amphistome fluke Gastrodiscoides hominis (Trematoda: Gastrodiscidae). Rev Iber Parasitol 66:75–81Google Scholar
  147. Muñoz-Antoli C, Sotillo J, Monteagudo C, Fried B, Marcilla A, Toledo R (2007) Development and pathology of Echinostoma caproni in experimentally infected mice. J Parasitol 93:854–859PubMedCrossRefPubMedCentralGoogle Scholar
  148. Muñoz-Antoli C, Cortés A, Martín-Grau C, Fried B, Esteban JG, Toledo R (2016a) Partial resistance to homologous challenge infections of the digenean Echinostoma caproni in ICR mice. J Helminthol 90:428–433PubMedCrossRefPubMedCentralGoogle Scholar
  149. Muñoz-Antoli C, Cortés A, Santano R, Sotillo J, Esteban JG, Toledo R (2016b) Interleukin-25 induces resistance against intestinal Trematodes. Sci Rep 6:34142PubMedPubMedCentralCrossRefGoogle Scholar
  150. Muttalib MA, Islam N (1975) Fasciolopsis buski in Bangladesh: a pilot study. J Trop Med Hyg 78:135–137PubMedPubMedCentralGoogle Scholar
  151. Niewiadomska K (2002) Family Diplostomidae Poirier, 1886. In: Gibson DI, Jones A, Bray RA (eds) Keys to the Trematoda, vol 1. CABI Publishing, Wallingford, pp 167–198CrossRefGoogle Scholar
  152. Park CJ, Kim J (2006) A human case of Echinostoma hortense infection diagnosed by endoscopy in area of southwestern Korea. Korean J Med 71:229–234Google Scholar
  153. Park KY, Lee KJ, Kim IS (2005) Reaction of mast cells and goblet cells in the small intestine of C57BL/6 and C3H/HeN mice infected with Echinostoma hortense. Korean J Biomed Lab Sci 11:259–266Google Scholar
  154. Pica R, Castellano C, Cilia C, Errico FO (2003) Intestinal fluke infections: the heterophyids. Clin Ter 154:61–63PubMedPubMedCentralGoogle Scholar
  155. Poland GA, Navin TR, Sarosi GA (1985) Outbreak of parasitic gastroenteritis among travelers returning from Africa. Arch Intern Med 145:2220–2221PubMedCrossRefPubMedCentralGoogle Scholar
  156. Pyo KH, Kang EY, Jung BK, Moon JH, Chai JY, Shin EH (2012) Depressed neuronal growth associated protein (GAP)-43 expression in the small intestines of mice experimentally infected with Neodiplostomum seoulense. Korean J Parasitol 50:89–93PubMedPubMedCentralCrossRefGoogle Scholar
  157. Quang TD, Duong TH, Richard-Lenoble D, Odermatt P, Khammanivong K (2008) [Emergence in humans of fascioliasis (from Fasciola gigantica) and intestinal distomatosis (from Fasciolopsis buski) in Laos]. Sante 18:119–124 (in French)Google Scholar
  158. Radomyos P, Bunnag D, Harinasuta T (1985) Report of Episthmium caninum (Verma, 1935) Yamaguti, 1958 (Digenea: Echinostomatidae) in man. Southeast Asian J Trop Med Public Health 16:508–511PubMedPubMedCentralGoogle Scholar
  159. Radomyos P, Bunnag D, Harinasuta C (1989) A new intestinal fluke, Plagiorchis harinasutai, n. sp. Southeast Asian J Trop Med Public Health 20:101–107PubMedPubMedCentralGoogle Scholar
  160. Radomyos P, Charoenlarp P, Harinasuta T (1991) Human Episthmium caninum (Digenea: Echinostomatidae) infection: report of two more cases. J Trop Med Parasitol 14:48–50Google Scholar
  161. Radomyos B, Wongsaroj T, Wilrairatana P, Radomyos P, Praevanich R, Meesomboon V, Jongsuksuntikul P (1998) Opisthorchiasis and intestinal fluke infections in northern Thailand. Southeast Asian J Trop Med Public Health 29:123–127PubMedPubMedCentralGoogle Scholar
  162. Rahman KM, Idris M, Khan AKA (1981) A study of fasciolopsiasis in Bangladesh. J Trop Med Hyg 84:81–86PubMedPubMedCentralGoogle Scholar
  163. Ryang YS, Ahn YK, Kim WT, Shin KC, Lee KW, Kim TS (1986) Two cases of human infection by Echinostoma cinetorchis. Kisaengchunghak Chapchi 24:71–76PubMedPubMedCentralGoogle Scholar
  164. Ryang YS, Yang EJ, Kim JL, Lee KJ, Sung HJ, Kim JB, Kim IS (2007) Immune response and inhibitory effect of ketotifen on the BALB/c and C3H/HeN mice infected with Echinostoma hortense. Parasitol Res 101:1103–1110PubMedCrossRefPubMedCentralGoogle Scholar
  165. Sah R, Khadka S, Hamal R, Poudyal S (2018) Human echinostomiasis: a case report. BMC Res Notes 11:17PubMedPubMedCentralCrossRefGoogle Scholar
  166. Sato M, Pongvongsa T, Sanguankiat S, Yoonuan T, Dekumyoy P, Kalambaheti T, Keomoungkhoun M, Phimmayoi I, Boupha B, Moji K, Waikagul J (2010) Copro-DNA diagnosis of Opisthorchis viverrini and Haplorchis taichui infection in an endemic area of Lao PDR. Southeast Asian J Trop Med Public Health 41:28–35PubMedPubMedCentralGoogle Scholar
  167. Saxton T, Fried B (2009) An update on metacercarial excystment of trematodes. Parasitol Res 105:1185–1191PubMedCrossRefPubMedCentralGoogle Scholar
  168. Sayasone S, Tesana S, Utzinger J, Hatz C, Akkhavong K, Odermatt P (2009a) Rare human infection with the trematode Echinochasmus japonicus in Lao PDR. Parasitol Int 58:106–109PubMedCrossRefPubMedCentralGoogle Scholar
  169. Sayasone S, Vonghajack Y, Vanmany M, Rasphone O, Tesana S, Utzinger J, Akkhavong K, Odermatt P (2009b) Diversity of human intestinal helminthiasis in Lao PDR. Trans R Soc Trop Med Hyg 103:247–254PubMedCrossRefPubMedCentralGoogle Scholar
  170. Sayasone S, Mak TK, Vanmany M, Rasphone O, Vounatsou P, Utzinger J, Akkhavong K, Odermatt P (2011) Helminth and intestinal protozoa infections, multiparasitism and risk factors in Champasack province, Lao People’s Democratic Republic. PLoS Negl Trop Dis 5:e1037PubMedPubMedCentralCrossRefGoogle Scholar
  171. Schell SC (1985) Trematodes of North America, north of Mexico. University Press of Idaho, IdahoGoogle Scholar
  172. Seo BS, Rim HJ, Lee CW (1964) Studies on the parasitic helmiths of Korea: I. Trematodes of rodents. Korean J Parasitol 2:20–26CrossRefGoogle Scholar
  173. Seo ES, Cho SY, Chai JY (1980) Studies on intestinal trematodes in Korea. I. A human case of Echinostoma cinetorchis infection with an epidemiological investigation. Seoul J Med 21:21–29Google Scholar
  174. Seo BS, Lee SH, Cho SY, Chai JY, Hong ST, Han IS, Sohn JS, Cho BH, Ahn SR, Lee SK, Chung SC, Kang KS, Shim HS, Hwang IS (1981) An epidemiologic study on clonorchiasis and metagonimiasis in riverside areas in Korea. Korean J Parasitol 19:137–150CrossRefGoogle Scholar
  175. Seo BS, Lee SH, Hong ST, Hong SJ, Kim CY, Lee HY (1982) Studies on intestinal trematodes in Korea: V. A human case infected by Fibricola seoulensis (Trematoda: Diplostomatidae). Korean J Parasitol 20:93–99CrossRefGoogle Scholar
  176. Seo BS, Lee SH, Chai JY, Hong SJ, Hong ST (1988) The life cycle and larval development of Fibricola seoulensis (Trematoda: Diplostomatidae). Korean J Parasitol 26:179–188CrossRefGoogle Scholar
  177. Seo M, Guk SM, Han ET, Chai JY (2003) Role of intestinal goblet cells in the expulsion of Gymnophalloides seoi from mice. J Parasitol 89:1080–1082PubMedCrossRefPubMedCentralGoogle Scholar
  178. Seo M, Chun H, Ahn G, Jang KT, Guk SM, Chai JY (2006) A case of colonic lymphoid tissue invasion by Gymnophalloides seoi in a Korean man. Korean J Parasitol 44:87–89PubMedPubMedCentralCrossRefGoogle Scholar
  179. Sheir ZM, Aboul-Enein ME (1970) Demographic, clinical and therapeutic appraisal of heterophyiasis. J Trop Med Hyg 73:148–152PubMedPubMedCentralGoogle Scholar
  180. Shin EH, Kim TH, Hong SJ, Park JH, Guk SM, Chai JY (2003) Effects of anti-allergic drugs on intestinal mastocytosis and worm expulsion of rats infected with Neodiplostomum seoulense. Korean J Parasitol 41:81–87PubMedPubMedCentralCrossRefGoogle Scholar
  181. Shin EH, Lee SH, Kim JL, Chai JY (2007) T-helper-1 and T-helper-2 immune responses in mice infected with the intestinal fluke Neodiplostomum seoulense: their possible roles in worm expulsion and host fatality. J Parasitol 93:1036–1045PubMedCrossRefPubMedCentralGoogle Scholar
  182. Shin EH, Im TK, Park YK, Cho J, Kim JL, Chai JY (2016) Fecundity reduction of BALB/c mice after survival from lethal Neodiplostomum seoulense infection. Parasitol Res 115:2051–2059PubMedCrossRefPubMedCentralGoogle Scholar
  183. Shoop WL (1989) Experimental human infection with Fibricola cratera (Trematoda: Neodiplostomidae). Korean J Parasitol 27:249–252CrossRefGoogle Scholar
  184. Shyu LY, Lee HH, Chen ER (1984) A preliminary study on epidemiology of fasciolopsiasis in Tainan Hsien, south Taiwan. Chin J Microbiol Immunol 17:118–120Google Scholar
  185. Sohn WM (2009) Fish-borne zoonotic trematode metacercariae in the Republic of Korea. Korean J Parasitol 47:S103–S113PubMedCrossRefGoogle Scholar
  186. Sohn WM, Ryang YS, Chai JY, Lee SH (1998) Discovery of Gymnophalloides seoi metacercariae in oysters from islands of the West Sea known as the habitats of paleartic oystercatchers. Korean J Parasitol 36:163–169PubMedPubMedCentralCrossRefGoogle Scholar
  187. Sohn WM, Kim HJ, Yong TS, Eom KS, Jeong HG, Kim JK, Kang AR, Kim MR, Park JM, Ji SH, Sinuon M, Socheat D, Chai JY (2011a) Echinostoma ilocanum infection in Oddar Meanchey Province, Cambodia. Korean J Parasitol 49:187–190PubMedPubMedCentralCrossRefGoogle Scholar
  188. Sohn WM, Chai JY, Yong TS, Eom KS, Yoon CH, Sinuon M, Socheat D, Lee SH (2011b) Echinostoma revolutum infection in children, Pursat Province, Cambodia. Emerg Infect Dis 17:117–119PubMedPubMedCentralCrossRefGoogle Scholar
  189. Sotillo J, Muñoz-Antoli C, Marcilla A, Fried B, Guillermo Esteban J, Toledo R (2007) Echinostoma caproni: kinetics of IgM, IgA and IgG subclasses in the serum and intestine of experimentally infected rats and mice. Exp Parasitol 116:390–398PubMedCrossRefGoogle Scholar
  190. Sotillo J, Valero L, Sánchez del Pino MM, Fried B, Esteban JG, Marcilla A, Toledo R (2008) Identification of antigenic proteins from Echinostoma caproni (Trematoda: Echinostomatidae) recognized by mouse immunoglobulins M, A and G using an immunoproteomic approach. Parasite Immunol 30:271–279PubMedCrossRefPubMedCentralGoogle Scholar
  191. Sotillo J, Trelis M, Cortés A, Fried B, Marcilla A, Esteban JG, Toledo R (2011) Th17 responses in Echinostoma caproni infections in hosts of high and low compatibility. Exp Parasitol 129:307–311PubMedCrossRefGoogle Scholar
  192. Sripa B, Kaewkes S, Intapan PM, Maleewong W, Brindley PJ (2010) Food-borne trematodiases in Southeast Asia epidemiology, pathology, clinical manifestation and control. Adv Parasitol 72:305–350PubMedCrossRefPubMedCentralGoogle Scholar
  193. Sukontason K, Unpunyo P, Sukontason KL, Piangiai S (2005) Evidence of Haplorchis taichui infection as pathogenic parasite: three case reports. Scand J Infect Dis 37:388–390PubMedCrossRefGoogle Scholar
  194. Takahashi S, Ishii T, Ueno N (1930) A human case of Echinostoma cinetorchis. Tokyo Iji Shinshi 2757:141–144Google Scholar
  195. Tantrawatpan C, Saijuntha W, Sithithaworn P, Andrews RH, Petney TN (2013) Genetic differentiation of Artyfechinostomum malayanum and A. sufrartyfex (Trematoda: Echinostomatidae) based on internal transcribed spacer sequences. Parasitol Res 112:437–441PubMedCrossRefPubMedCentralGoogle Scholar
  196. Thaenkham U, Phuphisut O, Pakdee W, Homsuwan N, Sa-nguankiat S, Waikagul J, Nawa Y, Dung do T (2011) Rapid and simple identification of human pathogenic heterophyid intestinal fluke metacercariae by PCR-RFLP. Parasitol Int 60:503–506PubMedCrossRefPubMedCentralGoogle Scholar
  197. Toledo R (2009) Immunology and pathology of echinostomes in the definitive host. In: Fried B, Toledo R (eds) The biology of Echinostomes. From the molecule to the community. Springer, New York, pp 185–206Google Scholar
  198. Toledo R, Esteban JG (2016) An update on human echinostomiasis. Trans R Soc Trop Med Hyg 110:37–45PubMedCrossRefGoogle Scholar
  199. Toledo R, Fried B (2005) Echinostomes as experimental models for interactions between adult parasites and vertebrate hosts. Trends Parasitol 21:251–254PubMedCrossRefGoogle Scholar
  200. Toledo R, Espert A, Muñoz-Antoli C, Marcilla A, Fried B, Esteban JG (2003) Development of an antibody-based capture enzyme-linked immunosorbent assay for detecting Echinostoma caproni (Trematoda) in experimentally infected rats: kinetics of coproantigen excretion. J Parasitol 89:1227–1231PubMedCrossRefPubMedCentralGoogle Scholar
  201. Toledo R, Espert A, Muñoz-Antoli C, Marcilla A, Fried B, Esteban JG (2004) Kinetics of Echinostoma caproni (Trematoda: Echinostomatidae) antigens in feces and serum of experimentally infected hamsters and rats. J Parasitol 90:752–758PubMedCrossRefPubMedCentralGoogle Scholar
  202. Toledo R, Espert A, Muñoz-Antoli C, Marcilla A, Fried B, Esteban JG (2005) Kinetics of antibodies and antigens in serum of mice experimentally infected with Echinostoma caproni (Trematoda: Echinostomatidae). J Parasitol 91:978–980PubMedCrossRefPubMedCentralGoogle Scholar
  203. Toledo R, Esteban JG, Fried B (2006a) Immunology and pathology of intestinal trematodes in their definitive hosts. Adv Parasitol 63:285–365PubMedCrossRefPubMedCentralGoogle Scholar
  204. Toledo R, Monteagudo C, Espert A, Fried B, Esteban JG, Marcilla A (2006b) Echinostoma caproni: intestinal pathology in the golden hamster, a highly compatible host, and the Wistar rat, a less compatible host. Exp Parasitol 112:164–171PubMedCrossRefPubMedCentralGoogle Scholar
  205. Toledo R, Esteban JG, Fried B (2009) Recent advances in the biology of echinostomes. Adv Parasitol 69:147–204PubMedCrossRefPubMedCentralGoogle Scholar
  206. Toledo R, Bernal MD, Marcilla A (2011) Proteomics of foodborne trematodes. J Proteome 74:1485–1503CrossRefGoogle Scholar
  207. Toledo R, Esteban JG, Fried B (2012) Current status of food-borne trematode infections. Eur J Clin Microbiol Infect Dis 31:1705–1718PubMedCrossRefGoogle Scholar
  208. Trelis M, Sotillo J, Monteagudo C, Fried B, Marcilla A, Esteban JG, Toledo R (2011) Echinostoma caproni (Trematoda): differential in vivo cytokine responses in high and low compatible hosts. Exp Parasitol 127:387–397PubMedCrossRefGoogle Scholar
  209. Trung Dung D, Van De N, Waikagul J, Dalsgaard A, Chai JY, Sohn WM, Murrell KD (2007) Fishborne zoonotic intestinal trematodes, Vietnam. Emerg Infect Dis 13:1828–1833PubMedCrossRefGoogle Scholar
  210. Uppal B, Wadhwa V (2005) Rare case of Metagonimus yokogawai. Indian J Med Microbiol 23:61–62PubMedCrossRefPubMedCentralGoogle Scholar
  211. Van Van K, Dalsgaard A, Blair D, Le TH (2009) Haplorchis pumilio and H. taichui in Vietnam discriminated using ITS-2 DNA sequence data from adults and larvae. Exp Parasitol 123:146–151PubMedCrossRefPubMedCentralGoogle Scholar
  212. Watthanakulpanich D, Waikagul J, Maipanich W, Nuamtanong S, Sanguankiat S, Pubampen S, Praevanit R, Mongkhonmu S, Nawa Y (2010) Haplorchis taichui as a possible etiologic agent of irritable bowel syndrome-like symptoms. Korean J Parasitol 48:225–229PubMedPubMedCentralCrossRefGoogle Scholar
  213. Weinstein MS, Fried B (1991) The expulsion of Echinostoma trivolvis and retention of Echinostoma caproni in the ICR mouse: pathological effects. Int J Parasitol 21:255–257PubMedCrossRefPubMedCentralGoogle Scholar
  214. Weng YL, Zhuang ZL, Jiang HP, Lin GR, Lin JJ (1989) Studies on ecology of Fasciolopsis buski and control strategy of fasciolopsiasis. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 7:108–111PubMedPubMedCentralGoogle Scholar
  215. Wongsawad P, Wongsawad C (2009) Development of PCR-based diagnosis of minute intestinal fluke, Haplorchis taichui. Southeast Asian J Trop Med Public Health 40:919–923PubMedPubMedCentralGoogle Scholar
  216. Wongsawad C, Kawin S, Wongsawad P, Paratasilpin T (2005) Some factors affecting Stellantchasmus falcatus metacercaria in laboratory. Southeast Asian J Trop Med Public Health 36:11711–11719Google Scholar
  217. Wongsawad C, Wongsawad P, Chai JY, Anuntalabhochai S (2009a) Haplorchis taichui, Witenberg, 1930: development of a HAT-RAPD marker for the detection of minute intestinal fluke infection. Exp Parasitol 123:158–161PubMedCrossRefPubMedCentralGoogle Scholar
  218. Wongsawad C, Wongsawad P, Chuboon S, Anuntalabhochai S (2009b) Copro-diagnosis of Haplorchis taichui infection using sedimentation and PCR-based methods. Southeast Asian J Trop Med Public Health 40:924–928PubMedPubMedCentralGoogle Scholar
  219. Xiao X, Wang TP, Lu DB, Gao JF, Xu LF, Wu WD, Mei JD, Xu FL (1992) The first record of human infection with Echinochasmus liliputanus. Chin J Parasitol Parasit Dis 10:132–135Google Scholar
  220. Xiao X, Dabing L, Tianping W, Gao J, Zhu C, Zhang B, An J, Pong H, Xu M, Wu W (1995) Studies on mode of human infection with Echinochasmus liliputanus. Chin J Parasitol Parasit Dis 13:197–199Google Scholar
  221. Yamaguti S (1971) Synopsis of digenetic trematodes of vertebrates. Keigaku Publishing Company, JapanGoogle Scholar
  222. Yamaguti S (1975) A synoptical review of the life histories of digenetic trematodes of vertebrates: with special reference to the morphology of their larval forms. Keigaku Publishing Company, JapanGoogle Scholar
  223. Yokogawa M, Harinasutam C, Charoenlarp P (1965) Hypoderaeum conoideum (Block, 1782) Diez, 1909, a common intestinal fluke of man in the north-east Thailand. Jpn J Parasitol 14:148–153Google Scholar
  224. Youn H (2009) Review of zoonotic parasites in medical and veterinary fields in the Republic of Korea. Korean J Parasitol 47:S133–S141PubMedPubMedCentralCrossRefGoogle Scholar
  225. Yu S, Mott K (1994) Epidemiology and morbidity of food-borne intestinal trematode infections. Trop Dis Bull 91:R125–R152Google Scholar
  226. Yu JR, Hong ST, Chai JY, Lee SH (1995) The effect of reinfection with Neodiplostomum seoulensis on the histopathology and activities of brush border membrane bound enzymes in the rat small intestine. Korean J Parasitol 33:37–43PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Rafael Toledo
    • 1
    Email author
  • Maria Alvárez-Izquierdo
    • 1
  • Carla Muñoz-Antoli
    • 1
  • J. Guillermo Esteban
    • 1
  1. 1.Área de Parasitología, Departamento de Farmacia y Tecnología Farmacéutica y Parasitología, Facultad de FarmaciaUniversidad de ValenciaValenciaSpain

Personalised recommendations