DOI QR코드

DOI QR Code

Morphology and Molecular Identification of Echinostoma revolutum and Echinostoma macrorchis in Freshwater Snails and Experimental Hamsters in Upper Northern Thailand

  • Butboonchoo, Preeyaporn (Department of Biology, Faculty of Science, Chiang Mai University) ;
  • Wongsawad, Chalobol (Department of Biology, Faculty of Science, Chiang Mai University) ;
  • Wongsawad, Pheravut (Department of Biology, Faculty of Science, Chiang Mai University) ;
  • Chai, Jong-Yil (Department of Tropical Medicine and Parasitology, Seoul National University College of Medicine)
  • 투고 : 2020.05.19
  • 심사 : 2020.09.22
  • 발행 : 2020.10.31

초록

Echinostome metacercariae were investigated in freshwater snails from 26 districts in 7 provinces of upper northern Thailand. The species identification was carried out based on the morphologies of the metacercariae and adult flukes harvested from experimental hamsters, and on nucleotide sequences of internal transcribed spacer 2 (ITS2) and nicotinamide adenine dinucleotide dehydrogenase subunit 1 (nad1) genes. Twenty-four out of 26 districts were found to be infected with echinostome metacercariae in freshwater snails with the prevalence of 40.4%. The metacercariae were found in all 6 species of snails, including Filopaludina martensi martensi (21.9%), Filopaludina doliaris (50.8%), F. sumatrensis polygramma (61.3%), Bithynia siamensis siamensis (14.5%), Bithynia pulchella (38.0%), and Anenthome helena (4.9%). The echinostome metacercariae found in these snails were identified as Echinostoma revolutum (37-collar-spined) and Echinostoma macrorchis (45-collar-spined) morphologically and molecularly. The 2-week-old adult flukes of E. revolutum revealed unique features of the cirrus sac extending to middle of the ventral sucker and smooth testes. E. macrorchis adults revealed the cirrus sac close to the right lateral margin of the ventral sucker and 2 large and elliptical testes with slight indentations and pointed posterior end of the posterior testis. The ITS2 and nad1 sequences confirmed the species identification of E. revolutum, and the sequences of E. macrorchis have been deposited for the first time in GenBank. The presence of the life cycle of E. macrorchis is a new record in Thailand and the snail F. doliaris as their second intermediate host seems to be new among the literature.

키워드

참고문헌

  1. Radomyos P, Radomyos B, Tungtrongchitr, A. Multi-infection with helminths in adults from northeast Thailand as determined by posttreatment fecal examination of adult worms. Trop Med Parasitol 1994; 45: 133-135.
  2. Toledo R, Fried B. Echinostomes as experimental models for interactions between adult parasites and vertebrate hosts. Trends Parasitol 2005; 21: 251-254. https://doi.org/10.1016/j.pt.2005.04.006
  3. Huffman JE, Fried B. Echinostoma and echinostomiasis. Adv Parasitol 1990; 29: 215-269. https://doi.org/10.1016/S0065-308X(08)60107-4
  4. Toledo R, Esteban JG, Fried B. Immunology and pathology of intestinal trematodes in their definitive hosts. Adv Parasitol 2006; 63: 285-365. https://doi.org/10.1016/S0065-308X(06)63004-2
  5. Toledo R, Monteagudo C, Espert A, Fried B, Esteban JG, Marcilla A. Echinostoma caproni: intestinal pathology in the golden hamster, a highly compatible host, and the Wistar rat, a less compatible host. Exp Parasitol 2006; 112: 164-171. https://doi.org/10.1016/j.exppara.2005.11.003
  6. Toledo R, Esteban JG. An update on human echinostomiasis. Trans R Soc Trop Med Hyg 2016; 110: 37-45. https://doi.org/10.1093/trstmh/trv099
  7. Chai JY, Sohn WM, Yong TS, Eom KS, Min DY, Hoang EH, Phommasack B, Insisiengmay B, Rim HJ. Echinostome flukes recovered from humans in Khammouane Province, Lao PDR. Korean J Parasitol 2012; 50: 269-272. https://doi.org/10.3347/kjp.2012.50.3.269
  8. Radomyos P, Bunnag D, Harinasuta T. Echinostoma ilocanum (Garrison, 1908) Odhner, 1911, infection in man in Thailand. Southeast Asian J Trop Med Public Health 1982; 13: 265-269.
  9. Saijuntha W, Duenngai K, Tantrawatpan C. Zoonotic echinostome infections in free-grazing ducks in Thailand. Korean J Parasitol 2013; 51: 663-667. https://doi.org/10.3347/kjp.2013.51.6.663
  10. Butboonchoo P, Wongsawad C. Occurrence and HAT-RAPD analysis of gastrointestinal helminths in domestic chickens (Gallus gallus domesticus) in Phayao Province, northern Thailand. Saudi J Biol Sci 2017; 24: 30-35. https://doi.org/10.1016/j.sjbs.2015.09.002
  11. Cho CM, Tak WY, Kweon YO, Kim SK, Choi YH, Kong HH, Chung DI. A human case of Echinostoma hortense (Trematoda: Echinostomatidae) infection diagnosed by gastroduodenal endoscopy in Korea. Korean J Parasitol 2003; 41: 117-120. https://doi.org/10.3347/kjp.2003.41.2.117
  12. Chang YD, Sohn WM, Ryu JH, Kang SY, Hong SJ. A human infection of Echinostoma hortense in duodenal bulb diagnosed by endoscopy. Korean J Parasitol 2005; 43: 57-60. https://doi.org/10.3347/kjp.2005.43.2.57
  13. Lo CT, Cross JH. Observation on the host-parasite relations between Echinostoma revolutum and lymnaeid snails. Chin J Microbiol 1975; 8: 241-252.
  14. Chung PR, Jung Y, Park YK, Hwang MK. Austropeplea ollula (Pulmonata: Lymnaeidae): a new molluscan intermediate host of a human intestinal fluke, Echinostoma cinetorchis (Trematoda: Echinostomatidae) in Korea. Korean J Parasitol 2001; 39: 247-253. https://doi.org/10.3347/kjp.2001.39.3.247
  15. Beaver PC. Experimental studies on Echinostoma revolutum (Froelich) a fluke from birds and mammals. In Buchholz JT, Tanner FW, Zeleny C eds, Illinois Biological Monographs. Urbana, USA. University of Illinois. 1937; 15: 1-96.
  16. Chai JY. Echinostomes in humans. In Fried B, Toledo R eds, The Biology of Echinostomes. New York. 2009, pp 147-183.
  17. Chantima K, Chai JY, Wongsawad C. Echinostoma revolutum: freshwater snail as the second intermediate hosts in Chiang Mai, Thailand. Korean J Parasitol 2013; 51: 183-189. https://doi.org/10.3347/kjp.2013.51.2.183
  18. Noikong W, Wongsawad C. Epidemiology and molecular genotyping of echinostome metacercariae in Filopaludina snails in Lamphun Province, Thailand. Asian Pac J Trop Biomed 2014; 1: 26-29. https://doi.org/10.1016/S1995-7645(13)60186-8
  19. Chomchoei N, Wongsawad C, Nantarat N. Investigation of cryptic diversity and occurrence of echinostome metacercariae infection in Anenthome helena (von dem Busch, 1847). Asian Pac J Trop Med 2018; 11: 590-596. https://doi.org/10.4103/1995-7645.244524
  20. Anucherngchai S, Panich W, Chontananarth T. The occurrence of the intestinal trematodes, Echinostoma revolutum (Froelich, 1802) infection in freshwater snails on the agricultural area of Chainat Province, Thailand. Khon Kaen Agr J 2018; 46 (suppl): 980-985 (in Thai).
  21. Anucherngchai S, Chontananarth T. Echinostoma revolutum: development of a high-performance DNA-specific primer to demonstrate the epidemiological situations of their intermediate hosts. Acta Trop 2019; 189: 46-53. https://doi.org/10.1016/j.actatropica.2018.09.014
  22. Chantima K, Suk-ueng K, Kampan M. Freshwater snail diversity in Mae Lao Agricultural Basin (Chiang Rai, Thailand) with a focus on larval trematode infections. Korean J Parasitol 2018; 56: 247-257. https://doi.org/10.3347/kjp.2018.56.3.247
  23. Toledo R. Echinostomes in the definitive host: a model for the study of host-parasite relationships. In Fried B, Toledo R eds. The Biology of Echinostomes. New York, USA. Springer. 2009, pp 89-109.
  24. Fujino T, Takahashi Y, Fried B. A comparison of Echinostoma trivolvis and E. caproni using random amplified polymorphic DNA analysis. J Helminthol 1995; 69: 263-267. https://doi.org/10.1017/S0022149X00014243
  25. Petrie JF, Burg EF, Cain GD. Molecular characterization of Echinostoma caproni and E. paraensei by random amplification of polymorphic DNA (RAPD) analysis. J Parasitol 1996; 82: 360-362. https://doi.org/10.2307/3284184
  26. Morgan JAT, Blair D. Relative merits of nuclear ribosomal internal transcribed spacers and mitochondrial CO1 and ND1 genes for distinguishing among Echinostoma species (Trematode). Parasitology 1998; 116: 289-297. https://doi.org/10.1017/S0031182097002217
  27. Georgieva S, Selbach C, Faltynkova A, Soldánavá M, Sures B, Skirnisson K, Kostadinova A. New cryptic species of the revolutum group of Echinostoma (Digenea: Echinostomatidae) revealed by molecular and morphological data. Parasit Vectors 2013; 6: 1-12. https://doi.org/10.1186/1756-3305-6-1
  28. Saijuntha W, Tantrawatpan C, Sithithaworn P, Duenngai K, Agatsuma T, Andrews RH, Petney TN. Genetic characterization and phylogenetic analysis of echinostomes from free-grazing ducks in Thailand using ribosomal DNA sequence. Southeast Asian J Trop Med Public Health 2014; 45: 1003-1010.
  29. Morgan JAT, Blair D. Nuclear rDNA ITS sequence variation in the trematode genus Echinostoma: an aid to establishing relationship within the 37 collar-spine group. Parasitology 1995; 11: 609-615. https://doi.org/10.1017/S003118200007709X
  30. Sorensen RE, Curtis J, Minchella DJ. Intraspecific variation in the rDNA ITS loci of 37 collar-spined echinostomes from North America: implications for sequence-based diagnoses and phylogenetics. J Parasitol 1998; 84: 992-997. https://doi.org/10.2307/3284633
  31. Kostadinova A, Herniou EA, Barrett J, Littlewood DTJ. Phylogenetic relationships of Echinostoma Rudolphi, 1809 (Digenea: Echinostomatidae) and related genera re-assessed via DNA and morphological analyses. Syst Parasitol 2003; 54: 159-176. https://doi.org/10.1023/A:1022681123340
  32. Humphries MM, Rancourt D, Farrar GJ, Kenna P, Hazel M, Bush RA, Sieving PA, Sheils DM, McNally N, Creighton P, Erven A, Boros A, Gulya K, Capecchi MR, Humphries P. Retinopathy induced in mice by targeted disruption of the rhodopsin gene. Nat Genet 1997; 15: 216-219. https://doi.org/10.1038/ng0297-216
  33. Kostadinova A, Gibson DI. Isthmiophora Lühe, 1909 and Euparyphium Dietz, 1909 (Digenea: Echinostomatidae) re-defined, with comments on their nominal species. Syst Parasitol 2002; 52: 205-217. https://doi.org/10.1023/A:1015789703396
  34. Maldonado Junior A, Zeitone BK, Amado LA, Rosa IF, Machado-Silva JR, Lanfredi RM Biological variation between two Brazilian geographical isolates of Echinostoma paraensei. J Helminthol 2005; 79: 345-351. https://doi.org/10.1079/JOH2005293
  35. Yamaguti S. Systema Helminthum, Vol I. The Digenetic Trematodes of Vertebrates. Part I and II. New York, USA. Interscience Publisher. 1958.
  36. Jones A, Bray RA, Gibson DI. Key to the Trematoda (Volume 2). London, UK. CABI Publishing and The Natural History Museum. 2005, pp 31-39.
  37. Chai JY, Sohn WM, Na BK, Nguyen VD. Echinostoma revolutum: metacercaria in Filopaludina snails from Nam Dinh Province, Vietnam, and adults from experimental hamsters. Korean J Parasitol 2011; 49: 449-455. https://doi.org/10.3347/kjp.2011.49.4.449
  38. Faltynkova A, Georgieva S, Soldanova M, Kostadinova A. A re-assessment of species diversity within the 'revolutum' group of Echinostoma Rudolphi, 1809 (Digenea: Echinostomatidae) in Europe. Syst Parasitol 2015; 90: 1-25. https://doi.org/10.1007/s11230-014-9530-3
  39. Nakataki M, Tantrawatpan C, Agatsuma T, Sugiura T, Duengai K, Sithithaworn P, Andrews RH, Petney TN, Saijuntha W. Mitochondrial DNA sequences of 37 collar-spined echinostomes (Digenea: Echinostomatidae) in Thailand and Lao PDR reveals presence of two species: Echinostoma revolutum and E. miyagawai. Infect Genet Evol 2015; 35: 56-62. https://doi.org/10.1016/j.meegid.2015.07.022
  40. Fried B, Graczyk TK. Recent advances in the biology of Echinostoma species in the 'revolutum'group. Adv Parasitol 2004; 58: 139-195. https://doi.org/10.1016/S0065-308X(04)58003-X
  41. Kanev I. Life-cycle, delimitation and redescription of Echinostoma revolutum (Froelich, 1802) (Trematoda: Echinostomatidae). Syst Parasitol 1994; 28: 125-144. https://doi.org/10.1007/BF00009591
  42. Sohn WM, Chai JY, Yong TS, Eom KS, Yoon CH, Sinuon M, Socheat D, Lee SH. Echinostoma revolutum infection in children, Pursat Province, Cambodia. Emerg Infect Dis 2011; 1: 117-119.
  43. Ando R, Ozaki Y. On four new species of trematodes of the family Echinostomatidae. Dobutsugaku Zasshi 1923; 35: 108-119 (in Japanese).
  44. Majima M. Echinostoma macrorchis found in a man. Tokyo Iji Shinshi 1927; 2552: 2260-2263.
  45. Shibue H. Studies on the trematodes of birds in Kyushu. Kurume Igakkai Zasshi 1954; 17: 178-183 (in Japanese).
  46. Okabe N, Okabe K. On a human case infected with three species of trematodes. Nippon Iji Shimpo 1972; 2531: 46-48 (in Japanese).
  47. Ito M, Itagaki T. Survey on wild rodents for endoparasites in Iwate Prefecture, Japan. J Vet Med Sci 2003; 65: 1151-1153. https://doi.org/10.1292/jvms.65.1151
  48. Fischthal JH, Kuntz RE. Additional records of digenetic trematodes of mammals from Taiwan. Proc Helminthol Soc Wash 1981; 48: 71-79.
  49. Sohn WM, Chai JY, Na BK, Yong TS, Eom KS, Park H, Min DY, Rim HJ. Echinostoma macrorchis in Lao PDR: metacercariae in Cipangopaludina snails and adults from experimentally infected animals. Korean J Parasitol 2013; 51: 191-196. https://doi.org/10.3347/kjp.2013.51.2.191
  50. Sohn WM, Na BK. Echinostoma macrorchis (Digenea: Echinostomatidae): Metacercariae in Cipangopaludina chinensis malleata snails and adults from experimental rats in Korea. Korean J Parasitol 2017; 55: 541-548. https://doi.org/10.3347/kjp.2017.55.5.541
  51. Sohn WM, Na BK, Lee D, Eom KS, Yong TS, Chai JY, Min DY. Echinostoma macrorchis metacercariae in Cipangopaludina chinensis malleata from Xiengkhuang Province, Lao PDR and morphologies of adults from experimental animals. Korean J Parasitol 2019; 57: 657-664. https://doi.org/10.3347/kjp.2019.57.6.657
  52. Kanev I, Fried B, Radev V. Collar spine models in the genus Echinostoma (Trematoda: Echinostomatidae). Parasitol Res 2009; 105: 921-927. https://doi.org/10.1007/s00436-009-1475-0
  53. Lo CT. Echinostoma macrorchis: life history, population dynamics of intramoluscan stages, and the first and second intermediate hosts. J Parasitol 1995; 81: 569-576. https://doi.org/10.2307/3283855
  54. Khalil M, Abaza MS. A new trematode parasite of the rat, Echinostoma aegyptiaca nov. sp. Rep Notes Public Health Labs Cairo 1924; 6: 187-189.
  55. Takahashi S. The life cycles of Echinostoma cinetorchis and E. macrorchis, particularly on their first and second intermediate hosts. Fukuoka Ika Daigaku Zasshi 1927; 20: 712-723 (in Japanese).
  56. Yamashita J. Echinostome. Progr Med Parasitol Japan 1964; 1: 289-313.
  57. Sohn WM. Life history of Echinoparyphium recurvatum (Trematoda: Echinostomatidae) in Korea. Korean J Parasitol 1998; 36: 91-98. https://doi.org/10.3347/kjp.1998.36.2.91
  58. Saijuntha W, Sithithawoorn P, Duenngai K, Kiatsopit N, Andrews RH, Petney TN. Genetic variation and relationship of four species of medically important echinostomes (Trematoda: Echinostomatidae) in South-East Asia. Infect Genet Evol 2011; 11: 375-381. https://doi.org/10.1016/j.meegid.2010.11.009