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Infection Status of Isthmiophora hortensis Metacercariae in Dark Sleepers, Odontobutis Species, from Some Water Systems of the Republic of Korea
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Korean J Parasito > Volume 56(6):2018 > Article
Sohn, Na, Cho, and Ju: Infection Status of Isthmiophora hortensis Metacercariae in Dark Sleepers, Odontobutis Species, from Some Water Systems of the Republic of Korea

Abstract

Present study was performed to survey on infection status of Isthmiophora hortensis (formerly Echinostoma hortense) metacercariae (IhMc) in dark sleepers, Odontobutis spp., from some water systems of the Republic of Korea. A total of 237 Odontobutis spp. was collected in the water systems of 5 rivers, i.e., Mangyeong-gang (gang means river), Geum- gang, Tamjin-gang, Seomjin-gang, and Nakdong-gang. They were all examined with artificial digestion method for 5 years (2013–2017). A total of 137 (57.8%) Odontobutis spp. were infected with 14.8 IhMc in average. The prevalence was the highest in Nakdong-gang areas (62.9%) and followed by in Mangyeong-gang (57.1%), Geum-gang (56.3%), Tamjingang (54.8%), and Seomjin-gang (53.9%) areas. Metacercarial densities were 28.1 (Geum-gang), 13.9 (Mangyeong-gang), 13.3 (Nakdong-gang), 13.1 (Tamjin-gang), and 2.3 (Seomjin-gang) per infected fish. Especially, in case of Yugucheon (cheon means stream), a branch of Geum-gang, IhMc were detected in all fish (100%) examined and their density was about 48 per fish. By the present study, it was confirmed that the infection status of IhMc is more or less different by the surveyed areas and the dark sleepers, Odontobutis spp., are suitable fish hosts of I. hortensis.

Isthmiophora hortensis (Digenea: Echinostomatidae) was redescribed by Kostadinova and Gibson [1] with a new combination from originally described as Echinostoma hortense in Japan [2]. Kostadinova and Gibson [1] clarified the validity of genus Isthmiophora, which had long been in the obscure taxonomic position in relation to the genus Euparyphium and additionally made a differential key to the species of Isthmiophora with the morphological characteristics of related worm samples. To support the taxonomic validity of this fluke, Sohn et al. [3] made the differential indices with variety of worm samples from the Republic of Korea (Korea). Since the original description from rats in Japan, this species of echinostome has been discovered in rats, dogs, cats, weasels, raccoons, striped field mice, a raccoon dog and a wild boar, which were naturally infected in Korea, Japan, China and Vietnam [312]. Human infections with this fluke were also reported in Japan, Korea and China [1319]. Especially in Korea, this echinostome is a dominant species with clinical importance [2028].
Several species of freshwater fishes, i.e., Misgurnus anguillicaudatus, Misgurnus mizolepis, Odontobutis obscura interrupta (O. interrupta), Moroco oxycephalus (Rhynchocypris oxycephalus), Coreoperca kawamebari and Squalidus coreanus (S. japonicus coreanus), yellowfin goby, Acanthogobius flavimanus, and tadpoles of Rana nigromaculata were reported as the second intermediate hosts and/or the source of human infection in Korea. Most of these reports were performed in limited areas and with small number of animals [2935]. Therefore, we examined the dark sleepers, Odontobutis spp., broadly collected from 13 sites in 5 rivers, i.e., Mangyeong-gang, Geum-gang, Tamjin-gang, Seomjin- gang and Nakdong-gang, of Korea.
Total 237 Odontobutis spp. were collected from 13 sites in 5 rivers, i.e., Mangyeong-gang (n=49), Geum-gang (n=32), Tamjin-gang (n=73), Seomjin-gang (n=13) and Nakdong-gang (n=70), and examined all with the artificial digestion method for 5 years (2013–2017) (Fig. 1). The number of fish examined by the surveyed sites was detailedly revealed in Table 1.
The metacercariae of I. hortensis (IhMc) were globular or elliptical, 143–165 (154) by 128–158 (144) μm in size, and have a double layered cyst wall, 27 collar spines including 4 end group ones in each side of the head crown, a ventral sucker transversely elliptical, 2-fold as larger as the oral sucker, and granules in the excretory bladder arranged in 2 rows of tube (Fig. 2).
A total of 137 (57.8%) Odontobutis spp. were infected with 14.8 IhMc in average. The prevalence was most high in Nakdong- gang areas (62.9%) and followed by it in Mangyeong-gang (57.1%), Geum-gang (56.3%), Tamjin-gang (54.8%) and Seomjin-gang (53.9%) areas. Metacercarial densities were 28.1 in Geum-gang, 13.9 in Mangyeong-gang, 13.3 in Nakdong-gang, 13.1 in Tamjin-gang and 2.3 per fish infected in Seomjin-gang respectively. Especially, in case of Yugucheon, a branch of Geumgang, IhMc were detected in all fish (100%) examined and their density was about 48 per fish. The infection status with IhMc in fish from 13 surveyed sites was detailedly designated in Table 1.
In the present study, it was confirmed that 2 species of dark sleepers, O. platycephala, and O. interrupta, are suitable fish hosts of I. hortensis although the infection status of IhMc is more or less different by the surveyed areas. Moreover, the prevalences and metacercarial densities of this study were much higher than those of previous studies. Ahn et al. [30] detected total 32 IhMc in 10 (27.8%) out of 36 dark sleepers, O. interrupta, from Seom-gang, a branch of Namhan-gang, in Wonseong-gun (gun=county), Gangwon-do (do=province). Ahn and Ryang [22] also detected IhMc in 4 (22.2%) out of 18 dark sleepers from Namhan-gang. Lee et al. [23] found IhMc in only 1 (2.3%) out of 44 dark sleepers from Cheongsong- gun, Gyeongsangbuk-do. Ryang [20] detected IhMc in 11 (20.3%) out of 54 dark sleepers from Chungju-ho (ho means lake) and the upper streams of Namhan-gang. In case of suitable fish host, muddy loach (Misgurnus anguillicaudatus), Chai et al. [29] reported that total 64 (41.6%) out of 154 loaches were infected with 1–29 (8.1 in average) IhMc per fish infected. Ahn and Ryang [22] detected IhMc in 106 (34.1%) out of 311 loaches from Namhan-gang. Lee et al. [23] found IhMc in 2 (10.5%) out of 19 loaches from Cheongsong-gun, Gyeongsangbuk- do. Ryang [20] detected IhMc in 30 (40.5%) out of 74 loaches from Chungju-ho and the upper streams of Namhan- gang. In another fish hosts of I. hortensis, M. mizolepis, R. oxycephalus, C. kawamebari, S. japonicus coreanus and A. flavimanus, small number of IhMc were detected in Korea [2935].
Some endemic foci of I. hortensis infections have been reported in Korea [2023]. Especially in the villages of Cheongsong- gun in Gyeongsangbuk-do, 59 (22.4%) out of 263 residents were positive with echinostome eggs and 1–649 (51 in average) adult worms of I. hortensis were collected from 35 egg-positive cases in the worm recovery after praziquantel treatment and MgSO4 purgation. As the source of human infections, the dark sleeper is most convincing among the second intermediate hosts in these endemic areas. It has been known that residents in inland of Korea frequently eat raw flesh of freshwater fishes such as Mandarin fish (Siniperca scherzeri), Korean aucha perch (Coreoperca herzi) and dark sleepers (O. platycephala and O. interrupta) [2023,30]. These fishes are powerful predators in the ecosystems of freshwater and presently eaten in raw by residents living in riverside areas of Korea. Therefore, Korean peoples pay attention to the raw consumption of dark sleepers, Odontobutis spp., to prevent the infections with this species of echinostomid fluke.

ACKNOWLEDGMENTS

This study was supported by an anti-communicable diseases control program, 2013-0171 (Studies on the biological resources of human infecting trematodes and their larval infections in intermediate hosts), 2014-E54002-00 (Investigation of fish-borne parasites and acquisition of their biological resources in the southern regions of Korea) and 2015-E54001-00 (Investigation of fish-borne parasites and acquisition of their biological resources in the easthern regions of Korea) of National Institute of Health (NIH), Korea Centers for Disease Control and Prevention (KCDCP). We thank Jung-A Kim and Hee-Joo Kim (Department of Parasitology and Tropical Medicine, Gyeongsang National University College of Medicine, Jinju, Korea), for their help in the examination of fish.

Conflict of interest

CONFLICT OF INTEREST
The authors declare that they have no conflict of interest with this article.

REFERENCES

1. Kostadinova A, Gibson DI. Isthmiophora Luhe, 1909 and Euparyphium Diet, 1909 (Digenea: Echinostomatidae) re-defined, with comments on their nominal species. Syst Parasitol 2002;52:205-217.
crossref pmid
2. Asada J. On a new echinostomatid trematode and its life history. Trans Jpn Soc Pathol 1926;16:293-294.

3. Sohn WM, Na BK, Shin SS. New definitive hosts and differential body indices of Isthmiophora hortensis (Digenea: Echinostomatidae). Korean J Parasitol 2017;55:287-294.
crossref pmid pmc pdf
4. Park JT. A rat trematode, Echinostoma hortense Asada, from Korea. Keijo J Med 1938;9:283-286.

5. Seo BS, Cho SY, Hong ST, Hong SJ, Lee SH. Studies on parasitic helminths of Korea V. Survey on intestinal trematodes of house rats. Korean J Parasitol 1981;19:131-136.
crossref
6. Cho SY, Kang SY, Ryang YS. Helminthes infections in the small intestine of stray dogs in Ejungbu City, Kyunggi Do, Korea. Korean J Parasitol 1981;19:55-59.
crossref
7. Chen HT. Fauna Sinica. Platyhelminthes, Trematoda, Digenea (I). Beijing, China. Science Press. 1985, pp 333-497.

8. Fan SQ, Sun MF. 1989. Echinostoma hortense. Bull Harbin Med Univ 1989;23:161.

9. Sato H, Suzuki K. Gastrointestinal helminths of feral raccoons (Procyon lotor) in Wakayama Prefecture, Japan. J Vet Med Sci 2006;68:311-318.
crossref pmid
10. Thi NLA, Madsen H, Thanh HD, Hoberg E, Dalsgaard A, Murrell KD. Evaluation of the role of rats as reservoir hosts for fish-borne zoonotic trematodes in two endemic northern Vietnam fish farms. Parasitol Res 2012;111:1045-1048.
crossref pmid
11. Sohn WM, Na BK, Song HJ, Kim CM, Nam GJ. Intestinal helminthic infections in striped field mice, Apodemus agrarius, from two southern regions of Korea. Korean J Parasitol 2014;52:419-423.
crossref pmid pmc
12. Shin SS, Oh DS, Ahn KS, Cho SH, Lee WJ, Na BK, Sohn WM. Zoonotic intestinal trematodes in stray cats (Felis catus) from riverside areas of the Republic of Korea. Korean J Parasitol 2015;53:209-213.
crossref pmid pmc
13. Seo BS, Hong ST, Chai JY, Lee SH. Studies on intestinal trematodes in Korea VII. A human case of Echinostoma hortense infection. Korean J Parasitol 1983;21:219-223.
crossref
14. Miyamoto K, Nakao M, Inaoka T. Studies on the zoonoses in Hokkaido, Japan. 5. On the epidemiological survey of Echinostoma hortense Asada, 1926. Jpn J Parasitol 1983;32:261-269.

15. Ryang YS, Ahn YK, Lee KW, Kim TS, Hhan MH. Two cases of natural human infection by Echinostoma hortense and its second intermediate host in Wonju area. Korean J Parasitol 1985;23:33-40.
crossref
16. Lee SK, Chung NS, Ko IH, Ko HI, Chai JY. Two cases of natural human infection by Echinostoma hortense. Korean J Parasitol 1986;24:77-81 (in Korean).
crossref
17. Chen XQ, Feng GX, Qian ZF. Survey on infection due to Echinostoma hortense in Liaoning Province. Chinese J Parasitol Parasit Dis 1993;11:226.

18. Huh S, Lee SU, Huh SC. A follow-up examination of intestinal parasitic infections of the army soldiers in Whachon-gun, Korea. Korean J Parasitol 1994;32:61-63.
crossref pmid
19. Hamamoto T, Kawasaki H, Maejima J, Hirai K. A case of Echinostoma hortense infection diagnosed by the upper gastrointestinal endoscopy. Nihon Shokakibyo Gakkai Zasshi 1997;94:487-491 (in Japanese).
pmid
20. Ryang YS. Studies on Echinostoma spp. in the Chungju Reservoir and upper stream of the Namhan River. Korean J Parasitol 1990;28:221-233 (In Korean).
crossref
21. Son WY, Huh S, Lee SU, Woo HC, Hong SJ. Intestinal trematode infections in the villagers in Koje-myon, Kochang-gun, Kyongsangnam-do, Korea. Korean J Parasitol 1994;32:149-155.
crossref pmid
22. Ahn YK, Ryang YS. Experimental and epidemiological studies on the life cycle of Echinostoma hortense Asada, 1926 (Trematoda: Echinostomatidae). Korean J Parasitol 1986;24:121-136 (in Korean).
crossref
23. Lee SK, Chung NS, Ko IH, Sohn WM, Hong ST, Chai JY, Lee SH. An epidemiological survey of Echinostoma hortense infection in Chongsong-gun, Kyongbuk Province. Korean J Parasitol 1988;26:199-206.
crossref
24. Chai JY, Hong ST, Lee SH, Lee GC, Min YI. A case of echinostomiasis with ulcerative lesions in the duodenum. Korean J Parasitol 1994;32:201-204.
crossref pmid
25. Lee OJ, Hong SJ. Gastric echinostomiasis diagnosed by endoscopy. Gastrointest Endosc 2002;55:440-442.
crossref pmid
26. 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.
crossref pmid pmc
27. 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.
crossref pmid pmc
28. Park CJ, Kim J. A human case of Echinostoma hortense infection diagnosed by endoscopy in area of southwestern Korea. Korean J Med 2006;71:229-234.

29. Chai JY, Hong SJ, Sohn WM, Lee SH, Seo BS. Studies on intestinal trematode in Korea. XVI. Infection status of loaches with the metacercariae of Echinostoma hortense. Korean J Parasitol 1985;23:18-23.
crossref
30. Ahn YK, Ryang YS, Chung PR, Lee KT. Echinostoma hortense meta-cercariae naturally encysted in Odontobutis obscura interrupta (a freshwater fish) and experimental infection to rats. Korean J Parasitol 1985;23:230-235 (in Korean).
crossref
31. Ryang YS, Ahn YK, Lee KW, Kim TS, Hhan MH. Two cases of natural human infection by Echinostoma hortense and its second intermediate host in Wonju area. Korean J Parasitol 1985;23:33-40.
crossref
32. Ryang YS. Studies on Echinostoma spp. in the Chungju Reservoir and upper streams of the Namhan River. Korean J Parasitol 1990;28:221-233.
crossref
33. Lee SH, Hwang SW, Sohn WM, Kho WG, Hong ST, Chai JY. Experimental life history of Echinostoma hortense. Korean J Parasitol 1991;29:161-172 (in Korean).
crossref
34. Sohn WM, Na BK, Cho SH. Echinostoma hortense and heterophyid metacercariae encysted in yellowfin goby, Acanthogobius flavimanus, from Shinan-gun and Muan-gun (Jeollanam-do), Korea. Korean J Parasitol 2009;47:307-310.
crossref pmid pmc
35. Sohn WM, Na BK, Cho SH, Ju JW, Lee SW, Seok WS. Infections with zoonotic trematode metacercariae in yellowfin goby, Acanthogobius flavimanus, from coastal areas of Republic of Korea. Korean J Parasitol 2018;56:259-265.
crossref pmid pmc pdf

Fig. 1
Two dark sleepers, Odontobutis interrupta, from Yugucheon in Gongju-si, Chungcheongnam-do, and Wicheon in Gunwi- gun, Gyeongsangbuk-do. The second intermediate host of I. hortensis identified in this study.
kjp-56-6-633f1.jpg
Fig. 2
Two metacercariae of I. hortensis collected from Korean dark sleeper, O. platycephala. They characteristically have an oral sucker (OS), ventral sucker (VS), 27 collar spines including 4 end group ones (encircled) in each side of the head crown and granules in the excretory bladder arranged in 2 rows of tube. Scale bar is 50 μm.
kjp-56-6-633f2.jpg
Table 1
Infection status of Isthmiophora hortensis metacercariae in dark sleepers, Odontobutis spp., from some water systems of Korea
Locality surveyed No. of fish examined No. of fish infected No. of metacercariae detected

Range Average
Soyangcheona 49 28 (57.1) 1–54 13.9

Geum-gang 32 18 (56.3) 1–123 28.1
 Cheonnae-gang (Geumsan) 22 8 (36.4) 1–13 3.5
 Yugucheon (Gongju) 10 10 (100) 5–123 47.7

Tamjin-gang 73 40 (54.8) 1–132 13.1
 Middle reaches (Jangheung) 49 23 (46.9) 1–132 20.3
 Lower reaches (Gangjin) 24 17 (70.8) 1–7 3.3

Seomjin-gang 13 7 (53.9) 1–4 2.3
 Seomjin-gang (Sunchang) 9 6 (66.7) 1–4 2.3
 Seomjin-gang (Gurye) 4 1 (25.0) - 2.0

Nakdong-gang 70 44 (62.9) 1–95 13.3
 Wicheon (Gunwi) 11 3 (27.3) 2–29 12.0
 Banbyeoncheon (Yeongyang) 4 3 (75.0) 2–21 8.7
 Yangcheon (Sancheong) 22 8 (36.4) 1–12 3.6
 Taehwa-gang (Ulju)b 9 7 (77.8) 1–91 29.4
 Hyeongsan-gang (Gyeongju) 21 20 (95.2) 1–95 12.9
 Osipcheon (Yeongdeok) 3 3 (100) 3–25 10.7

Total 237 137 1–132 14.8

a A branch of Mangyeonggang located in Wanju-gun, Jeollabuk-do.

b 6 fish collected from Cheokgwacheon (a branch of Taehwagang) located in Ulju-gun, Ulsan Metropolitan City.

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