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Intestinal trematodes of humans in Korea: Metagonimus, heterophyids and echinostomes
J Y Chai and S H Lee
Department of Parasitology and Institute of Endemic Diseases, Seoul National University College of Medicine, Seoul 110-460, Korea.
Abstract
Ten species of the trematode family Heterophyidae (Metagonimus yokogawai, M. takahashii, Heterophyes nocens, H. heterophyes, H. dispar, Heterophyopsis continua, Pygidiopsis summa, Stellantchasmus falcatus, Centrocestus armatus and Stictodora fuscatum), and 3 species of the family Echinostomatidae (Echinostoma hortense, E. cinetorchis and Echinochasmus japonicus) have been found to infect humans in Korea. Biological and epidemiological studies on the above species have shown that Metagonimus, heterophyids and echinostomes are all prevalent indigenously in Korea except H. heterophyes and H. dispar, of which the human cases were infected when they came to the Middle East. Various kinds of fish have been proven to be the source of human infection with these flukes. For example, fresh water fish such as the sweetfish, carp, loach, etc., were found to carry the metacercarial stage of M. yokogawai, M. takahashii, C. armatus, E. hortense, E. cinetorchis and/or E. japonicus. Brackish water fish such as the mullet, perch and goby, were verified to be the second intermediate host of H. nocens, H. continua, P. summa, S. falcatus and/or S. fuscatum. Among the intestinal flukes, M. yokogawai is the most prevalent species in Korea.
Figures
Fig. 1 Metagonimus yoiogawai, bentral view, acetocarmine stained, recovered from a man. Note the location of the ventral sucker(VS) and two tests (T).
Fig. 2 Map of the geographical distribution of M. yokogawai in Korea, based of the metacercarial infection in the sweetfish (Redrawn from Seo et al., 1982 & Song et al., 1985).
Fig. 3 Section of M. yokogawai in the jejunum, (A) at an early stage (3-day) of infection in d dog (X200), and(B) at a later stage (2-week) of infection in a rat (×100) (Chai, 1979). Note villous atrophy (B) and crypt hyperplasia (A&B) of the host's jejunal mucosa. H-E stain.
Fig. 4 Eggs of M. yokogawai, obtained from the uterus of several adult worms.
Fig. 5 Metagonimus takahashii, ventral view, fresh preparation from a man. Note the ventral sucker (VS), two separately located testes (T), uterine tubule crossing over the two testes, and posteriormost extension of vitellaria.
Figs. 6-7 Heterophyes nocens (Fig. 6) and H. heterophyes (Fig. 7), ventral view, fresh preparations from a man (Chai et al., 1985b) and another (Chai et al., 1986a). Note the ventral sucker (VS) and other organs, that show no special difference between the two species, except in the morphology of the genital sucker (GS) (for detail see Fig. 8-9).
Figs. 8-9 Close-up view of the ventral sucker (VS) and genital sucker (GS) of H. nocens (Fig. 8) and H. heterophyes (Fig. 9). The number of rodlets on the gonotyl (GS) is about 53 from the former (Fig. 8) and about 76 from the latter (Fig. 9).
Figs. 10-11 Heterophyes dispar, ventral view of a whole worm (Fig. 10) and a close-up view (Fig. 11) of the vental sucker (VS) and genital sucker (GS), fresh preparation from a man (Chai et al., 1986a). Note the small size of the genital sucker (GS) (Fig. 10) compared with th large ventral one (VS) and small number (about 30) of rodlets on the gonotyl (Fig. 11).
Fig. 12 Heterophyopsis continua, ventral view, acetocarmine stained, recovered from a man (Seo et al., 1984b). Note the elongated body shape, ventral sucker (VS), genital sucker (GS), and two obliquely tandem testes (T).
Fig. 13 Pygidiopsis summa, ventral view, fresh preparation from an experimentally infected rat (10-day old worm) (Chai et al., 1986b). Note the slightly submedian ventral sucker (VS) and associated genital apparatus, forming together a ventrogenital apparatus (VGA). Also see the two side-by-side testes (T).
Fig. 14 Stellantchasmus falcatus, ventral view, fresh preparation from a patient (Seo et al., 1984a). Note th submedian ventral sucker (VS), elongated sac-like seminal vesicle (SV), and two side-by-side testes (T).
Fig. 15 Centrocestus armatus, ventral view, drawing from a specimen recovered from a man (Hong et al., 1988). Note the circumoral spines characteristic of this genus.
Fig. 16 Stictodora fuscatum, ventral view, fresh specimen from a patient in a southwestern coastal area (Chai et al., to be published). Note the characteristic features of the ventrogenital sac (VGS), metraterm (MT) containing an egg, two obliquely located testes (T), and distribution of the vitellaria.
Fig. 17 Echinostama hortense, 28-day (A), 42-day (B) and 150-day worm (C) grown in experimental rats, acetocarmine stained (Seo et al., 1985a). Note the large ventral sucker (VS), submedian location of the ovary (Ov), and two slightly lobulated tandem testes (T).
Fig. 18 Section of the duodenum of a rat 22 days after experimental infection with E. hortense (Lee et al., 1990). Note a worm sucking at a villus with its oral sucker armed with collar spines (arrows). The host mucosa shows villous atrophy and crypt hyperplasia, with inflammatory reactions. H-E stain. ×100.
Fig. 19 Echinostoma cinetorchis, ventral view of two adult worms, grown in experimental rats 16 days after infection, acetocarmine stained (Seo et al., 1984c). Note a worm (A) that has two testes (T) one of which moved to an abnormal location and another that has only one testis (T).
Fig. 20 Echinochasmus japonicus, ventral view of a fresh specimen (A) recovered from a naturally infected chicken and dorsal view of an acetocarmine stained specimen (B) from an experimentally infected chick. Note the arrangement of 24 collar spines (arrows) which is discontinued dorsally, large ventral sucker (VS), two tandem tested (T) and small uterus with only one egg (E) each.
Tables
Table 1 Human intestinal flukes which belong to the family Heterophyidae or Echinostomatidae in Korea
References
1.
Africa CM, et al. Phil J Sci 1935;57:253–267.
2.
Africa CM, et al. Acta Medica Philippina, Monographic Series NO 1940;1:1–132.
3.
Ahn YK. New Med J 1983;26:135–139.
4.
Ahn YK, et al. J Wonju Med Coll 1988;1:137–152.
5.
Ahn YK, Ryang YS. [Epidemiological studies on Metagonimus infection along the Hongcheon river, Kangwon province]. Korean J Parasitol 1988;26(3):207–213.
6.
Ahn YK, Ryang YS, Chai JY, Sohn WM. [Cercarial shedding of Echinostoma cinetorchis and experimental infection of the cercariae to several kinds of snails]. Korean J Parasitol 1989;27(3):203–211.
7.
Alicata JE, et al. J Am Med Ass 1938;110:1100–1101.
8.
Ando R, et al. Dobutsugaku Zasshi 1923;35:108–119.
9.
Asada J. Trans Jap Path Soc 1926;16:293–294.
10.
Castro GA. Immunophysiology of enteric parasitism. Parasitol Today 1989;5(1):11–19.
11.
Chai JY. Seoul J Med 1979;20:104–117.
12.
Chai JY, Cho SY, Seo BS. Study on Metagonimus yokogawai(Katsurada, 1912) in Korea: IV. An epidemiological investigation along Tamjin River basin, South Cholla Do, Korea. Korean J Parasitol 1977;15(2):115–120.
13.
Chai JY, Hong SJ, Lee SH, Seo BS. Stictodora sp. (Trematoda: Heterophyidae) recovered from a man in Korea. Korean J Parasitol 1988;26(2):127–132.
14.
Chai JY, Hong SJ, Sohn WM, Lee SH, Seo BS. Studies on intestinal tematodes in Korea: XVI. Infection status of loaches with the metacercariae of Echinostoma hortense. Korean J Parasitol 1985;23(1):18–23.
15.
Chai JY, et al. Seoul J Med 1985;26:197–200.
16.
Chai JY, Hong SJ, Son DW, Lee SH, Seo BS. [Metacercariae of Echinochasmus japonicus encysted in a fresh water fish, Pseudorasbora parva, and their development in experimental mice]. Korean J Parasitol 1985;23(2):221–229.
17.
Chai JY, Seo BS, Lee SH. Studies on intestinal trematodes in Korea XI. Two cases of human infection by Heterophyes heterophyes nocens. Korean J Parasitol 1984;22(1):37–42.
18.
Chai JY, Seo BS, Lee SH. Study On Metagonimus Yokogawai(Katsurada, 1912) In Korea Vii. Susceptibility Of Various Strains Of Mice To Metagonimus Infection And Effect Of Prednisolone. Korean J Parasitol 1984;22(2):153–160.
19.
Chai JY, Seo BS, Lee SH, Hong SJ, Sohn WM. Human infections by Heterophyes heterophyes and H. dispar imported from Saudi Arabia. Korean J Parasitol 1986;24(1):82–86.
20.
Chai JY, Seo BS, Lee SH, Hong ST. Growth and development of Pygidiopsis summa in rats and mice with a supplementary note on its morphological characters. Korean J Parasitol 1986;24(1):55–62.
21.
Chai JY, Sohn WM. Identification of Stellantchamus falcatus Metacercariae encysted in mullets in Korea. Korean J Parasitol 1988;26(1):65–68.
22.
Chai JY, et al. Seou J Med 1989;30:139–142.
23.
Chi JG, et al. J Korean Med Sci 1988;3:171–177.
24.
Cho SY, et al. Arzneim-Forsch/Drug Res 1984;34:1211–1213.
25.
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(1):55–59.
26.
Cho SY, Kim SI. Plecoglossus altivelis as a new fish intermediate host of Heterophyopsis continua. Korean J Parasitol 1985;23(1):173–174.
27.
Cho SY, Kim SI, Earm YE, Ho WK. A preliminary observation on watery content of small intestine in Metagonimus yokogawai infected dog. Korean J Parasitol 1985;23(1):175–177.
28.
Cho SY, Kang SY, Kim SI. Analysis of antigen specificity using monoclonal and polyclonal antibodies to Cysticercus cellulosae by enzyme-linked immunoelectrotransfer blot technique. Korean J Parasitol 1987;25(2):159–167.
29.
Choi DW, Lee JT, Hwang HK, Shin YD. [Studies Of The Larval Trematodes From Brackish Water Fishes: 2. Observation On Metagonimus Yokogawai Katsurada, 1912]. Korean J Parasitol 1966;4(1):33–37.
30.
Chun SK. Bull Pusan Fish Coll 1960;3:31–39.
31.
Chun SK. Bull Pusan Fish Coll 1960;3:40–44.
32.
Chun SK. Bull Pusan Fish Coll 1963;5:1–5.
33.
Chun SK. Bull Pusan Fish Coll 1964;6:1–14.
34.
Eom KS, Rim HJ, Jang DH. A Study On The Parasitic Helminths Of Domestic Duck(Anas Platyrhynchos Var. Domestica Linnaeus) In Korea. Korean J Parasitol 1984;22(2):215–221.
35.
Eom KS, Son SY, Lee JS, Rim HJ. Heterophyid trematodes (Heterophyopsis continua, Pygidiopsis summa and Heterophyes heterophyes nocens) from domestic cats in Korea. Korean J Parasitol 1985;23(2):197–202.
36.
Eom KS, et al. Heterophyid trematodes (Heterophyes heterophyes and H. dispar) human infections imported from Sudan to Korean. Korean J Parasit 1985;23:360–361.
37.
Faust EC, et al. J Parasitol 1926;13:91–131.
38.
Hong SJ, Lee SH, Chai JY, Seo BS. Recovery rate, growth and development of Heterophyopsis continua in experimental chicks. Korean J Parasitol 1990;28(1):53–62.
39.
Hong SJ, Seo BS, Lee SH, Chai JY. A human case of Centrocestus armatus infection in Korea. Korean J Parasitol 1988;26(1):55–60.
40.
Hong SJ, Woo HC, Kim IT. [Study on Centrocestus armatus in Korea. I. Infection status of Zacco platypus and Z. temminckii with the metacercariae of C. armatus]. Korean J Parasitol 1989;27(1):41–46.
41.
Hong ST, Chai JY, Lee SH. Ten human cases of Fibricola seoulensis infection and mixed one with Stellantchasmus and Metagonimus. Korean J Parasitol 1986;24(1):95–97.
42.
Ito J. Progress of Med Parasit in Japan 1964;1:314–393.
43.
Jang YK, Kang SY, Kim SI, Cho SY. In situ posture of anterior body of Metagonimus yokogawai in experimentally infected dog. Korean J Parasitol 1985;23(2):203–213.
44.
Kagei N, et al. Jap J Parasitol 1964;13:472–478.
45.
Jang YK, Kang SY, Kim SI, Cho SY. In situ posture of anterior body of Metagonimus yokogawai in experimentally infected dog. Korean J Parasitol 1985;23(2):203–213.
46.
Kawahara S, et al. Tokyo Iji Shinshi 1933;(2840):1794–1796.
47.
Kim CH, Kim NM, Lee CH, Park JS. [Studies on the Metagonimus fluke in the Daecheong reservoir and the upper stream of Geum river, Korea]. Korean J Parasitol 1987;25(1):69–82.
48.
Lee JB, Chi JG, Lee SK, Cho SY. Study On The Pathology Of Metagonimiasis In Experimentally Infected Cat Intestine. Korean J Parasitol 1981;19(2):109–129.
49.
Rhee JK, Lee HI, Baek BK, Kim PG. [Survey On Encysted Cercariae Of Trematodes From Fresh-Water Fishes In Mangyeong Riverside Area]. Korean J Parasitol 1983;21(2):187–192.
50.
Rhee JK, Rim MH, Baek BK, Lee HI. [Survey On Encysted Cercaria Of Trematodes From Fresh-Water Fishes In Tongjin Riverside Areas In Korea]. Korean J Parasitol 1984;22(2):190–202.
51.
Lee SH, et al. J Korean Soc Chemother 1984;2:167–171.
52.
Lee SH, Chai JY, Hong ST, Sohn WM. Experimental life history of Echinostoma cinetorchis. Korean J Parasitol 1990;28(1):39–44.
53.
Lee SH, Hwang SW, Chai JY, Seo BS. Comparative Morphology Of Eggs Of Heterophyids And Clonorchis Sinensis Causing Human Infections In Korea. Korean J Parasitol 1984;22(2):171–180.
54.
Lee SH, Noh TY, Sohn WM, Kho WG, Hong ST, Chai JY. [Chronological observation of intestinal lesions of rats experimentally infected with Echinostoma hortense]. Korean J Parasitol 1990;28(1):45–52.
55.
Lee SH, Seo BS, Chai JY, Hong SJ. [Study on Metagonimus yokogawai(Katsurada, 1912) in Korea VII. Electron microscopic observation on the tegumental structure. Korean J Parasitol 1984;22(1):1–10.
56.
Lee SK, Chung NS, Ko IH, Ko HI, Sohn WM. [A case of natural human infection by Echinostoma cinetorchis]. Korean J Parasitol 1988;26(1):61–64.
57.
Lee SK, Chung NS, Ko IH, Sohn WM, Hong ST, Chai JY, Lee SH. [An epidemiological suryey of Echinostoma hortense infection in Chongsong-gun, Kyongbuk province]. Korean J Parasitol 1988;26(3):199–206.
58.
Loose A. Centralbl Bakt Orig 1902;32:886–891.
59.
Miyamoto K, et al. Jpn J Parasitol 1983;32:261–269.
60.
Noda K. The larval development of Stellantchasmus falcatus (Trematoda: Heterophyidae) in the first intermediate host. J Parasitol 1959;45:635–642.
61.
Onji Y, et al. Chiba Igaku Semmon Gakko Zasshi 1916;81&82:229–249.
62.
Park JT. Keijo J Med 1938;9:283–286.
63.
Radomyos P, et al. Jpn J Parasitol 1990;39:7–11.
64.
Rho IH, et al. Chung-Ang J Med 1984;9:67–77.
65.
Rim HJ, Chu DS, Lee JS, Joo KH, Won CY. [Anthelmintic Effects Of Various Drugs Against Metagonimiasis]. Korean J Parasitol 1978;16(2):117–122.
66.
Ryang YS. [Studies on Echinostoma spp. in the Chungju Reservoir and upper streams of the Namhan River]. Korean J Parasitol 1990;28(4):221–233.
67.
Ryang YS, Ahn KY, Kim WT, Shin KC, Lee KW, Kim TS. [Two cases of human infection by Echinostoma cinetorchis. Korean J Parasitol 1986;24(1):71–76.
68.
Saito S. Proc of Jap Parasite Taxon Morphol Conf 1984;2:1–6.
69.
Seo BS. Seoul J Med 1990;31:61–96.
70.
Seo BS, et al. Seoul J Med 1986;27:125–134.
71.
Seo BS, et al. Seoul J Med 1980;21:21–29.
72.
Seo BS, et al. Seoul J Med 1980;21:30–38.
73.
Seo BS, Cho SY, Hong ST, Hong SJ, Lee SH. Studies On Parasitic Helminths Of Korea 5.Survey On Intestinal Trematodes Of House Rats. Korean J Parasitol 1981;19(2):131–136.
74.
Seo BS, Chun KS, Chai JY, Hong SJ, Lee SH. Studies on intestinal trematodes in Korea: XVII. Development of egg lying capacity of Echinostoma hortense in albino rats and human experimental infection. Korean J Parasitol 1985;23(1):24–32.
75.
Seo BS, et al. Seoul J Med 1981;22:228–235.
76.
Seo BS, et al. Seoul J Med 1981;22:236–242.
77.
Seo BS, Hong ST, Chai JY, Lee SH. [Study On Metagonimus Yokogawai (Katsurada, 1912) In Korea: VI.The Geographical Distribution Of Metacercarial Infection In Sweetfish Along The East And South Coast]. Korean J Parasitol 1982;20(1):28–32.
78.
Seo BS, Hong ST, Chai JY, Lee SH. Studies On Intestinal Trematodes In Korea: VIII. A Human Case Of Echinostoma Hortense Infection. Korean J Parasitol 1983;21(2):219–223.
79.
Seo BS, et al. Seoul J Med 1985;26:207–212.
80.
Seo BS, Lee SH, Chai JY, Hong SJ. Studies on intestinal trematodes in Korea [XII. Two cases of human infection by Stellantchasmus falcatus. Korean J Parasitol 1984;22(1):43–50.
81.
Seo BS, Lee SH, Chai JY, Hong SJ. Studies on intestinal trematodes in Korea XIII. Two cases of natural human infection by Heterophyopsis continua and the status of metacercarial infection in brackish water fishes. Korean J Parasitol 1984;22(1):51–60.
82.
Seo BS, Lee SH, Chai JY, Hong SJ. Studies on intestinal trematodes in Korea XX. Four cases of natural human infection by Echinochasmus japonicus. Korean J Parasitol 1985;23(2):214–220.
83.
Seo BS, Lee SH, Chai JY, Hong ST, Hong SJ. Efficacy Of Mebendazole In Treatment And Control Of Trichuriasis In Korea. Korean J Parasitol 1983;21(1):95–101.
84.
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. An Epidemiologic Study On Clonorchiasis And Metagonimiasis In Riverside Areas In Korea. Korean J Parasitol 1981;19(2):137–150.
85.
Seo BS, Park YH, Chai JY, Hong SJ, Lee SH. [Studies On Intestinal Trematodes In Korea Xiv. Infection Status Of Loaches With Metacercariae Of Echinostoma Cinetorchis And Their Development In Albino Rats]. Korean J Parasitol 1984;22(2):181–189.
86.
Seo BS, Rim HJ, Lee CW. Studies on the parasitic helmiths of Korea: I. Trematodes of rodents. Korean J Parasitol 1964;2(1):20–26.
87.
Seo BS, et al. Seoul J Med 1971;12:234–241.
88.
Soh CT, et al. Yonsei Rep Trop Med 1976;7:3–16.
89.
Sohn WM, et al. Inje Med J 1989;10:443–452.
90.
Sohn WM, Chai JY, Lee SH. A human case of Stellantchasmus falcatus infection. Korean J Parasitol 1989;27(4):277–279.
91.
Song CY, Lee SH, Jeon SR. [Studies on the intestinal fluke, Metagonimus yokogawai Katsurada, 1912 in Korea Geographical distribution of sweetfish and infection status with Metagonimus metacercaria in south-eastern area of Korea]. Korean J Parasitol 1985;23(1):123–138.
92.
Takahashi S. Okayama Igakkai Zasshi 1929;41(12):2687–2755.
93.
Takahashi S. Okayama Igakkai Zasshi 1929;41:1502–1513.
94.
Takahashi S. Okayama Igakkai Zasshi 1929;4:1759–1771.
95.
Tanabe H. Kyoto Igaku Zasshi 1922;19:239–252.
96.
Tanabe H. Nippon Byori Gakkai Kaishi 1926;16:295–296.
97.
Tani S. Jpn J Parasitol 1976;25:262–273.
98.
Ujiie N. Taiwan Igakkai Zasshi 1936;35:535–546.
99.
Yamaguti S. Jap J Med Sci VI 1939;1:131–151.
100.
Yeo TO, et al. Seoul J Med 1971;12:259–267.
101.
Yokogawa M, et al. Jap J Parasitol 1965;14:577–585.
102.
Zhu D, et al. J Parasitol Parasitic Dis 1986;4:1–4.
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