Abstract
Fishborne trematode (FBT) metacercariae were investigated in yellowfin goby, Acanthogobius flavimanus, collected from Shinan-gun and Muan-gun, Jeollanam-do (province), Korea. All collected fishes were examined using the artificial digestion method. In all of 15 gobies from Aphae-myeon in Shinan-gun, metacercariae of Stictodora spp. (334 metacercariae/fish), Heterophyes nocens (153/fish), and Heterophyopsis continua (20/fish) were detected. In 2 of 14 gobies from Jido-myeon in Shinan-gun, 8 Echinostoma hortense metacercariae in total were detected. In 15 gobies from Haeje-myeon in Muan-gun, the metacercariae of H. continua were found in 100%, Stictodora spp. in 86.7%, and H. nocens in 6.7% of fish examined. The average numbers of metacercariae per infected fish were 23.3 (H. continua), 416.0 (Stictodora spp.), and 2.0 (H. nocens), respectively. The metacercariae of E. hortense found in gobies were elliptical, with 150 × 138 µm in average size, and had 27 collar spines on the head crown. The above results suggest that yellowfin gobies from 2 localities may be the potential infection sources of FBT. Moreover, it is proved for the first time that the yellowfin goby, A. flavimanus, acts as a second intermediate host for E. hortense.
-
Key words: Echinostoma hortense, heterophyids, fishborne trematode metacercariae, yellowfin goby, Shinan-gun, Muan-gun
More than 50 million people are currently estimated to be infected with intestinal trematodes, including at least 18 million people infected by fishborne trematodes (FBT) around the world. Heterophyid (Heterophyidae) and echinostomatid flukes (Echinostomatidae) are regarded as the most important groups found in the intestinal tract of humans [
1,
2]. With regard to heterophyids, 10 species in 7 genera, i.e.
Metagonimus yokogawai,
Metagonimus takahashii,
Metagonimus miyatai,
Heterophyes nocens,
Heterophyopsis continua,
Stellantchasmus falcatus,
Pygidiopsis summa,
Centrocestus armatus,
Strictodora fuscata, and
Stictodora lari, have been reported as human-infecting species in the Republic of Korea [
2]. Among them, 6 species, namely,
H. nocens,
H. continua,
P. summa,
S. falcatus,
S. fuscata, and
S. lari, are infected by consumption of raw flesh of estuarine fish [
1,
2]. Among these fish hosts, yellowfin goby,
Acanthogobius flavimanus, are sometimes heavily infected with the metacercariae of heterophyid flukes, and are popularly eaten raw by many residents in coastal areas of Korea [
3-
7]. However, echinostomatid metacercariae have never been reported from yellowfin gobies in the Republic of Korea. Therefore, we performed an epidemiological survey to know the infection status of FBT metacercariae in yellowfin gobies collected in Shinan-gun and Muan-gun, Jeollanam-do (province), the Republic of Korea.
On September 2006, 14-15 gobies were collected, and examined by artificial digestion method (
Table 1). Trematode metacercariae were segregated, collected under a stereomicroscope, and categorized according to measurements and morphological characteristics. Infection rates and intensities were then calculated. A total of 8
Echinostoma hortense metacercariae collected in gobies from Jido-myeon in Shinan-gun were used to experimentally infect a rat to obtain adult worms. Two weeks after the infection, 4 adult flukes were recovered from the small intestine of the rat, which were fixed in 10% neutral buffered formalin, and stained with Semichon's acetocarmine in order to observe their morphological characteristics.
Metacercariae of
H. nocens,
H. continua, and
Stictodora spp. were detected in all of 15 gobies caught from Aphae-myeon in Shinan-gun. The average numbers of metacercariae per infected fish were 153 (
H. nocens), 20 (
H. continua), and 334 (
Stictodora spp.) respectively. A total of 11
P. summa metacercariae were collected in only 1 goby from Aphae-myeon (
Table 2). In 2 of 14 gobies from Jido-myeon in Shinan-gun, 8
E. hortense metacercariae were detected; however, no other kinds of metacercariae were found in 14 gobies from Jido-myeon. In 15 gobies from Haeje-myeon in Muan-gun, the metacercariae of
H. continua were found in 100%,
Stictodora spp. in 86.7%, and
H. nocens in 6.7% of gobies examined. The average numbers of metacercariae per infected fish were 23.3 (
H. continua), 416 (
Stictodora spp.), and 2.0 (
H. nocens), respectively (
Table 2).
The metacercariae of
E. hortense found in gobies were elliptical, 140-163 × 130-143 µm (mean 150 × 138 µm) in size, and had 27 collar spines on the head crown, and excretory granules were arranged posteriorly in V-shape from the pharynx level (
Fig. 1). Adults of
E. hortense recovered from an experimental rat at 2 week after infection were 8.20-9.05 × 1.35-1.63 mm (mean 8.72 × 1.51 mm) in size, had 27 collar spines, and the other morphological characteristics, for example, the right-side deviated round ovary, lobular testes, diffusely distributed vitellaria, and intrauterine eggs, were compatible with previous studies. One adult specimen (Semichon's acetocarmine stained) of
E. hortense is deposited in Invertebrate Research Division, National Institute of Biological Resources, Korea (NIBRIV0000128379).
It has been proved for the first time in this study that the yellowfin goby,
A. flavimanus, acts as a second intermediate host for
E. hortense. As the second intermediate hosts of this fluke, several species of freshwater fish, i.e. muddy loach (
Misgurnus anguillicaudatus), Chinese muddy loach (
Misgurnus mizolepis), dark sleeper (
Odontobutis interrupta), Chinese minnow (
Rhynchocypris oxycephalus), Japanese aucha perch (
Coreoperca kawamebari), short barbel gudgeon (
Squalidus japonicus coreanus), and some species of amphibians, frogs (
Rana nigromaculata,
Rana rugosa,
Rana catesbiana), salamanders (
Hynobius naevius,
Hynobius nebulosus), and toad (
Bufo vulgaris japonicus) have been reported in Japan, Korea, and China [
8-
15].
Human infections with
E. hortense have been reported in Japan, Korea, and China [
16-
18]. Especially in the Republic of Korea, a 22.4% (59/263) egg-positive rate was reported in a survey of residents in Cheongsong-gun, Gyeongsangbuk-do [
13], and recently, clinical cases have been diagnosed occasionally by the gastroduodenal endoscopy [
19-
23].
Endemic foci of heterophyid flukes are scattered around the southwestern coastal areas and islands, especially in Shinan-gun and Muan-gun (Jeollanam-do), Korea. Some species of estuarine fish, including
Lateolabrax japonicus,
Clupanodon punctatus,
Mugil cephalus, and
A. flavimanus, have been reported as sources of human infection in these endemic areas [
2]. Among these fish hosts,
A. flavimanus is sometimes heavily infected with heterophyid metacercariae, and are popularly eaten raw by many residents in southwestern coastal areas [
3-
7].
Several species of heterophyid fluke metacercariae, i.e.
H. nocens,
H. continua,
P. summa,
S. fuscata,
S. lari, and
Acanthotrema felis, were found in the yellowfin gobies in the Republic of Korea [
3-
7,
24]. In the present study, metacercariae of
H. nocens,
H. continua,
Stictodora spp., and
P. summa were detected, and especially, high infection rates and intensities were revealed in gobies from Aphae-myeon in Shinan-gun. Metacercariae of
H. continua,
Stictodora spp., and
H. nocens were detected in 15 gobies from Haeje-myeon in Muan-gun. However, except for
E. hortense, no other metacercariae were found in 14 gobies from Jido-myeon in Shinan-gun. These findings together suggest that those who consume raw yellowfin gobies,
A. flavimanus, from Shinan-gun and Muan-gun are at a high risk of infection with heterophyid flukes and
E. hortense.
ACKNOWLEDGEMENTS
This study was supported by an Anti-Communicable Diseases Control Program of the National Institute of Health (NIH 348-6111-215), Ministry of Health and Welfare, the Republic of Korea. We thank Miss A-Ra Cho and Hae-In Ryu, Department of Parasitology, Gyeongsang National University School of Medicine, Jinju, Korea, for their help in examination of fish.
References
- 1. Chai JY. Intestinal flukes. Food-Borne Parasitic Zoonoses: Fish and Plant-Borne Parasites. World Class Parasites. 2007, Vol. 11:New York, USA. Springer; pp 53-115.
- 2. Chai JY, Lee SH. Food-borne intestinal trematode infections in the Republic of Korea. Parasitol Int 2002;51:129-154.
- 3. Seo BS, Hong ST, Chai JY, Cho SY. Studies on intestinal trematodes in Korea. IV. Geographical distribution of Pygidiopsis and Heterophyes metacercariae. Seoul J Med 1981;22:236-242.
- 4. Chai JY, Park SK, Hong SJ, Choi MH, Lee SH. Identification of Stictodora lari (Heterophyidae) metacercariae encysted in the brackish water fish, Acanthogobius flavimanus. Korean J Parasitol 1989;27:253-259.
- 5. Sohn WM, Chai JY, Lee SH. Stictodora fuscatum (Heterophyidae) metacercariae encysted in gobies, Acanthogobius flavimanus. Korean J Parasitol 1994;32:143-148.
- 6. Sohn WM, Moon BC. Infection status with the metacercariae of heterophyid trematode in mullet and goby collected from western coastal areas of Cholla-do, Korea. J Biomed Lab Sci 2001;7:31-37.
- 7. Kim DG, Kim TS, Cho SH, Song HJ, Sohn WM. Heterophyid metacercarial infections in brackish water fishes from Jinju-man (Bay), Kyongsangnam-do, Korea. Korean J Parasitol 2006;44:7-13.
- 8. Asada S. On a new echinostomatid trematode and its life history. Trans Jap Pathol Soc 1926;16:293-294.
- 9. Tani S. Studies on Echinostoma hortense (Asada, 1926) (1) Species identification of human echinostomiasis and its infection source. Jpn J Parasitol 1976;25:262-273.
- 10. Tani S. Studies on Echinostoma hortense (Asada, 1926) (2) The intermediate and final hosts in Akita Prefecture. Jpn J Parasitol 1976;25:461-467.
- 11. Chai JY, Hong SJ, Sohn WM, Lee SH, Seo BS. Studies on intestinal trematodes in Korea. XVI. Infection status of loaches with the metacercariae of Echinostoma hortense. Korean J Parasitol 1985;23:18-23.
- 12. Ryang YS, Ahn YK, Lee KW, Kim TS, Hahn 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.
- 13. 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.
- 14. Ryang YS. Studies on Echinostoma spp. in the Chungju Reservoir and upper streams of the Namhan River. Korean J Parasitol 1990;28:221-233.
- 15. Yu SH, Mott KE. Epidemiology and morbidity of food-borne intestinal trematode infections. Trop Dis Bull 1994;91:R125-R152.
- 16. 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.
- 17. 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.
- 18. Chen XQ, Feng GX, Qian ZF. Survey on infection due to Echinostoma hortense Asada in Liaoning Province. Chinese J Parasitol Parasit Dis 1993;11:226.
- 19. 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.
- 20. Lee SJ, Hong SJ. Gastric echinostomiasis diagnosed by endoscopy. Gastrointestinal Endoscopy 2002;55:440-442.
- 21. 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.
- 22. 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.
- 23. 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.
- 24. Sohn WM, Han ET, Seo M, Chai JY. Identification of Acanthotrema felis (Digenea: Heterophyidae) metacercariae encysted in the brackish water fish Acanthogobius flavimanus. Korean J Parasitol 2003;41:101-105.
Fig. 1The metacercariae of Echinostoma hortense detected in an yellowfin goby, Acanthogobius flavimanus, from Jido-myeon, Shinan-gun (Jeollanam-do), Korea. They are elliptical with 150 × 138 µm average size, and had an oral sucker (OS) and 27 collar spines (arrow marks) in the head crown, and excretory granules (EG) located posteriorly in V-shape from the pharynx level. Scale bar = 50 µm.
Table 1.The yellowfin goby, Acanthogobius flavimanus, collected in Shinan-gun and Muan-gun (Jeollanam-do), Korea
Table 1.
|
Locality fish collected |
No. of examined |
Length (cm)
|
Weight (g)
|
|
Range |
Average |
Range |
Average |
|
Aphae-myeon, Shinan-gun |
15 |
15.0-18.5 |
16.5 |
23.7-50.9 |
34.0 |
|
Jido-myeon, Shinan-gun |
14 |
17.5-27.0 |
21.6 |
36.5-124.2 |
75.0 |
|
Haeje-myeon, Muan-gun |
15 |
14.2-22.7 |
19.1 |
22.9-78.4 |
52.1 |
Table 2.Infection status of heterophyid metacercariae in gobies from Aphae-myeon, Shinan-gun and Haeje-myeon, Muan-gun (Jeollanam-do), Korea
Table 2.
|
Locality of fish & trematode species |
No. (%) infected |
No. of metacercariae detected
|
|
Total |
Range |
Average |
|
Aphae-myeon, Shinan-gun |
|
|
|
|
|
Stictodora spp. |
15 (100) |
5,012 |
12-982 |
334.1 |
|
Heterophyes nocens
|
15 (100) |
2,298 |
12-282 |
153.2 |
|
Heterophyopsis continua
|
15 (100) |
299 |
3-75 |
19.9 |
|
Pygidiopsis summa
|
1 (6.7) |
11 |
- |
11.0 |
|
Haeje-myeon, Muan-gun |
|
|
|
|
|
Heterophyopsis continua
|
15 (100) |
350 |
1-102 |
23.3 |
|
Stictodora spp. |
13 (86.7) |
5,407 |
9-3,226 |
415.9 |
|
Heterophyes nocens
|
1 (6.7) |
2 |
- |
2.0 |
Citations
Citations to this article as recorded by
- Clonorchis sinensis and Echinostoma hortense detected by endoscopy and molecular characterization: two case reports and update on diagnosis
Lijia Wen, Benhe Wang, Hui Zhang
Frontiers in Medicine.2025;[Epub] CrossRef - The Nuclear Ribosomal Transcription Units of Two Echinostomes and Their Taxonomic Implications for the Family Echinostomatidae
Yu Cao, Ye Li, Zhong-Yan Gao, Bo-Tao Jiang
Biology.2025; 14(8): 1101. CrossRef - Reliability of heterophyid antigens in heterologous protection against human schistosomiasis
Alaa H. A. Hegazy, Lamia A. Galal, Tasneem M. Hassan, Refaat M. A. Khalifa
Journal of Parasitic Diseases.2020; 44(2): 349. CrossRef - Infections with Zoonotic Trematode Metacercariae in Yellowfin Goby, Acanthogobius flavimanus, from Coastal Areas of Republic of Korea
Woon-Mok Sohn, Byoung-Kuk Na, Shin-Hyeong Cho, Jung-Won Ju, Soon-Won Lee, Won-Seok Seok
The Korean Journal of Parasitology.2018; 56(3): 259. CrossRef - Infection Status of Isthmiophora hortensis Metacercariae in Dark Sleepers, Odontobutis Species, from Some Water Systems of the Republic of Korea
Woon-Mok Sohn, Byoung-Kuk Na, Shin-Hyeong Cho, Jung-Won Ju
The Korean Journal of Parasitology.2018; 56(6): 633. CrossRef - Fishborne zoonotic heterophyid infections: An update
Jong-Yil Chai, Bong-Kwang Jung
Food and Waterborne Parasitology.2017; 8-9: 33. CrossRef - Pygidiopsis summa (Digenea: Heterophyidae): Status of Metacercarial Infection in Mullets from Coastal Areas in the Republic of Korea
Woon-Mok Sohn, Byoung-Kuk Na, Shin-Hyeong Cho, Won-Ja Lee, Mi-Yeoun Park, Soon-Won Lee, Seung-Bong Choi, Beom-Nyung Huh, Won-Seok Seok
The Korean Journal of Parasitology.2016; 54(4): 497. CrossRef - Studies on some fish parasites of public health importance in the southern area of Saudi Arabia
Mokhtar Ibrahim Khalil, Ismail Saad El-Shahawy, Hussein Saad Abdelkader
Revista Brasileira de Parasitologia Veterinária.2014; 23(4): 435. CrossRef - Infection Status of Estuarine Fish and Oysters with Intestinal Fluke Metacercariae in Muan-gun, Jeollanam-do, Korea
Shin-Hyeong Cho, In-Sang Kim, Eun-Jung Hwang, Tong-Soo Kim, Byoung-Kuk Na, Woon-Mok Sohn
The Korean Journal of Parasitology.2012; 50(3): 215. CrossRef - Seasonal features of Heterophyopsis continua metacercariae in perches, Lateolabrax japonicus, and infectivity to the final host
Sung-Jong Hong
Parasitology Research.2012; 110(3): 1209. CrossRef - Epidemiological Survey on the Infection of Intestinal Flukes in Residents of Muan-gun, Jeollanam-do, the Republic of Korea
Shin-Hyeong Cho, Pyo-Yun Cho, Dong-Min Lee, Tong-Soo Kim, In-Sang Kim, Eun-Jung Hwang, Byoung-Kuk Na, Woon-Mok Sohn
The Korean Journal of Parasitology.2010; 48(2): 133. CrossRef - Fish-borne Zoonotic Trematode Metacercariae in the Republic of Korea
Woon-Mok Sohn
The Korean Journal of Parasitology.2009; 47(Suppl): S103. CrossRef
