intestinal trematodes infecting humans in korea

INTESTINAL TREMATODES INFECTING HUMANS IN KOREA

Jong- Yil Chai and Soon-Hyung Lee

Department of Parasitology and Institute of Endemic Diseases, Seoul National UniversityCollege of Medicine, Seoul 110-460, Korea.

Abstract. Sixteen species of intestinal trematodes have been recovered from humans in Korea.They include 10 species of the family Heterophyidae (Metagonimus yokogawai, M. takahashii,Heterophyes nocens, H. heterophyes, H. dispar, Heterophyopsis continua, Pygidiopsis summa, Stellant-chasmus falcatus, Centrocestus armatus, and Stictodora fuscatum); one species of Diplostomidae(Fibricola seoulensis); three species of Echinostomatidae (Echinostoma hortense, E. cinetorchis, andEchinochasmus japonicus); one species of Plagiorchiidae (Plagiorchis sp.), and one species ofGymnophallidae (Gymnophalloides sp.).

Biological and epidemiological studies have shown that all of these species are endemic to Koreaexcept H. heterophyes and H. dispar, which were imported from the Middle East, and Plagiorchissp., which has not been found in Korea. Several fresh water fish were found carrying metacercarialstages of M. yokogawai, M. takahashii, C. armatus, E. hortense, E. cinetorchis and E. japonicus.Brackish water fish were found to be the second intermediate host of H. nocens, H. continua, P.summa, S. falcatus, and/or S. fuscatum. Terrestrial snakes were the second intermediate (or paratenic)host of F. seoulensis. Among these intestinal flukes, M. yokogawai is the most common one in Korea.

INTRODUCTION

Among the trematodes infecting the humanhost, the liver fluke (Clonorchis sinensis) and thelung fluke (Paragonimus westermani), trans-mitted by crabs or crayfish, are important para-sites because of their relatively high prevalenceand wide geographical distribution in Korea.Recently, however, trematodes infecting theintestinal tract of animals and man (intestinalflukes) have become important, because theycause food-borne parasitic zoonoses. There are16 species that belong to five families (Table 1).This paper reviews the biological and epidemio-logical aspects of intestinal trematodes affectinghumans in Korea.

FAMILY HETEROPHYIDAE

Metagonimus yokogawai (Katsurada, 1912) Katsu-rada, 1912

This is the most common species of intestinaltrematode reported in Korea. The presence ofhuman infection with this fluke was suggestedearlier in Korea by the recovery of eggs fromfecal examinations, but the identification ofadult worms was not made until 1971 (Seo et ai,

1971). Streams in eastern and southern coastalareas, where sweetfish (Plecoglossus altivelis) arefound, are known to be the endemic foci ofmetagonimiasis. The overall egg positive rate ofriverside people was estimated at 4.8% (Seo etal, 1981c). The Sumjin, Tamjin, and BoseongRivers, and Geoje Island are highly endemicareas where the villagers have 10-20% eggpositive rates (Chai et al, 1977; Seo et ai, 1981c).

Morphologically, this species is distinguishedfrom M. takahashii by the location and arrange-ment of two testes and size of the eggs (Saito,1984). Fresh water snails, Semisulcospira coreanaand S. libertina, are the first intermediate host ofM. yokogawai. Second intermediate hosts includethe sweetfish, the dace (Tribolodon taczanowskii)(Choi et ai, 1966), and the perch (Lateolabraxjaponicus) (Ahn, 1983). Dogs, rats, and cats arereported natural final hosts, but their significanceas a source of human infection has not beenclarified.

The intestinal histopathology was studied inrats, cats or dogs (Chai, 1979; Kang et aI, 1983),with the pathology characterized by villousatrophy and crypt hyperplasia, and with variabledegrees of inflammatory cell infiltrations. Experi-

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FOOD - BORNE PARASITIC ZOONOSIS

Table 1Intestinal flukes infecting humans in Korea

Family species Second IH Egg size (urn) Adult size (mm)

HeterophyidaeMetagonimus yokogawai fresh water fish 28-30 x 16-17 1.0-2.0 x 0.4-0.6

(sweet fish)M takahashii fresh water fish 32-36 x 18-23 0.8-1.5 x 0.4-0.7

(carps)Heterophyes nocens brackish water fish 25-28 x 14-16 0.9-1.6 x 0.5-0.8

(mullets, gobies)H.heterophyes * brackish water fish 28-30 x 15-17 1.0-1.7 x 0.3-0.4

(mullets)H.dispar* brackish water fish 19-25 x 13-15 1.0-1.7 x 0.5-0.6

(mullets)Heterophyopsis continua brackish water fish 25-27 x 14-16 2.7-2.8 x 0.5-0.6

(perches, gobies)Pygidiopsis summa brackish water fish 19-26 x 12-14 0.5-0.8 x 0.3-0.4

(mullets, gobies)Stellantchasmus faloatus brackish water fish 22-23 x 11-12 0.4-0.7 x 0.3-0.4

(mullets)Centrocestus armatus fresh water fish 28-32 x 16-17 0.4-0.6 x 0.2-0.3

(carps)Stictodora fuscatum brackish water fish 34-38 x 20-23 0.9-1.0 x 0.3-0.4

(mullets)Diplostomidae

Fibricola seoulensis tadpoles and frogs 81-102 x 51-63 0.8-1.2 x 0.4-0.5terrestrial snakes

EchinostomatidaeEchinostoma hortense fresh water fish 105-128 x 43-68 8.2-14.0 x 0.9-1.6

(loaches, carps)E.cinetorchis fresh water fish 95-105 x 60-68 8.6-15.0 x 2.0-2.4

(loaches, large snails)Echinochasmus japonicus fresh water fish 85 x 56 0.5-1.0 x 0.3

(carps)Plagiorchiidae

Plagiorchis sp. fresh water fish 32-38 x 20-24 2.9-3.0 x 0.8-1.0(?)

GymnophallidaeGymnophalloides sp. marine bivalves 20-25 x 12-14 0.4-0.5 x 0.2-0.3

(oyster)

* Cases were imported from Africa and Middle East.

mental immunosuppression of the host canprolong the survival time of the parasite in thehost intestine (Chai et al, 1984b).

The most frequent complaints from humanswere abdominal pain, diarrhea and lethargy (Cho

et ai, 1984). The diagnosis is usually based onrecovery of eggs in feces; however, eggs may beabsent in light infections with less than 100worms. The ELISA serological test may behelpful for such cases (Chai et al, 1989). The

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INTESTINAL TREMATODES IN KOREA

drug of choice is praziquantel, a single oral doseof 10-20 mg/kg, which gave an efficacy of 95-100% (Rim et al, 1978). Bithionol and niclosa-mide are also of therapeutic value.

Metagonimus takahashii Suzuki, 1930

This species differs from M. yokogawai inthe position of the anterior testis (more separa-tion from posterior one), distribution of vitellinefollicles (more posterior and more abundant), andlarger size of eggs (32-36 urn) (Saito, 1984).However, because of the presence of an inter-mediate type, Metagonimus Miyata type (Saito,1984), the validity of this needs further clarifi-cation. M. takahashii has been reported fromJapan and Korea.

The presence of this species in Korea wasfirst reported by Chun (1960a) who recoveredadult worms from experimentally infected rabbitsfed metacercariae obtained from crucian carps.Human infections were reported in 1985 and1988 (Ahn and Ryang, 1988), however, theywere not based on a detailed morphologicaldiagnosis of worms.

Unlike M. yokogawai, M. takahashii (and/orMetagonimus Miyata type) is distributed alongsmall streams in inland areas of Korea. Thesnail host is S. coreana or Koreanomelanisnodifila (Cho et ai, 1984), and the fish host is,Carrasius carrasius (Chun, 1960a), Cyprinuscarpio, Pseudorasbora parva, or Zacco platypus(for Miyata type). There have been few reportson reservoir hosts.

Heterophyes nocens Onji and Nishio, 1916

This species is morphologically close to H.heterophyes, which is prevalent in Egypt andthe Middle East, but it differs by the morphologyof genital sucker, especially the number of rodletson the gonotyl: 50-62 in H. nocens and 70-85in H. heterophyes. This species has been reportedfrom Korea and Japan.

In Korea, the metacercariae were first foundin 1978-1979 (Seo et ai, 1980b) from mullets(Mugil cephalus) captured in three southerncoastal areas. Before 1990, human infectionswith this fluke were verified in 13 personsfrom scattered areas (Seo et ai, 1981a; Chai etai, 1984a, 1985b; Sohn et ai, 1989). In April 1990,

a highly endemic area of H. nocens infectionwas discovered from a southwestern coastalisland, where as many as 42% of the populationwas found infected (to be published).

The first intermediate host is suspected to bea brackish water snail. The second intermediatehost is brackish water fish, such as mullets orgobies (Acanthogobius flavimanus) (Seo et ai,1981b). Domestic cats were found naturallyinfected (Eom et ai, 1985).

Heterophyopsis continua (Onji and Nishio, 1916)Yamaguti, 1958

This species, first found in cats experimentallyfed mullets (Mugi/ cephalus) harboring metacer-cariae, and is now known to be distributed inKorea, Japan and China (Seo et ai, 1984b).

The presence of H. continua in Korea wasfirst verified by Chun (1960b) who observedmetacercariae in the flesh of perch and gobies.Two cases of human infection in Korea werereported by Seo et al (1984b); two additionalcases were described by Hong and Han (1989).The first intermediate host is not known inKorea. The second intermediate hosts are perch,gobies, shad (Clupanodon punctatus) (Chun 1960b), and sweetfish (Cho and Kim, 1985). Do-mestic cats were reported to be naturally infected(Eom et ai, 1985). Dogs (Seo et ai, 1984b) andchicks (Hong et ai, 1990) have been experi-mentally infected.

Pygidiopsis summa Onji and Nishio, 1916

This species was first found in Japan in dogsfed mullets harboring metacercariae, and it isnow known to be distributed in Korea. P.summa is differentiated from P. genata inthe morphology of the ventral sucker, genitalapparatus, and ceca (Chai et al, 1986).

The presence of P. summa in Korea was firstdescribed by Chun (1963), who observed metacer-cariae from the gill and muscle of mullets. Humaninfection was first reported from 8 persons livingin a salt farm village who ate raw mullets (Seo etai, 1981a).

The first intermediate host is Cerithidea(= Tympanotonus) sp. (unpublished data). Thesecond intermediate hosts are mullets and gobies

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(Seo et al, 1981b). Natural infection of domesticcats was reported (Eom et al, 1985). In experi-mental rats and mice, the middle intestine ismost frequently infected, and like M. yokogawai,the worms cause severe villous atrophy and crypthyperplasia with inflammation of the mucosa(Seo et al, 1986).

Stellantchasmus falcatus Onji and Nishio, 1916

Human infections with S. falcatus have beenreported from several Asian-Pacific countries,including Korea (Seo et ai, 1984a; Hong et ai,1986). The life cycle was studied in Hawaii; thefirst intermediate host is Stenomelania newcombior Thiara granifera (Noda, 1959) and the secondintermediate host is the mullet (Chai and Sohn,1988). In Korea, the snail host is not yet known.

Centrocestus armatus (Tanabe, 1922)

This fluke was first described by Tanabe(1922) from dogs, cats, rabbits, rats, and mice,fed cyprinoid fish harboring metacercariae. Anexperimental infection was reported in Japan(Tanabe, 1922) and a natural infection was foundin Korea (Hong et al, 1988).

The first intermediate host is Semisulcospirasp. in Japan (Takahashi, 1929). Fresh waterfish, such as Zacco platypus, Rhodeus ocellatus,Gobius similis, Pseudorasbora parva, Pelteo-bagrus fulvidraco, and several other species,were reported to harbor the metacercariae ofC. armatus in Korea (Lee et ai, 1984 a, b). Arecent field survey on metacercarial infection offish hosts (Hong et al, 1989b) showed thatZ. platypus and Z. temminckii caught in the largerivers of south Korea were heavily infected.

Stictodorafuscatum Onji and Nishio, 1916

This species was originally described by Onjiand Nishio (1916) from cats fed infected mullets(M. cephalus) in Japan. Human infection withStictodora sp. was reported from a young Koreanfond of eating raw mullets or gobies (Chai et ai,1988).

FAMIL Y DIPLOSTOMIDAE

Fibricola seoulensis Seo, Rim and Lee, 1964

This species was first described by Seo et ai,

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(1964) from the small intestine of house ratscaptured in Seoul and are now known to bedistributed almost all over the country (Seo,1990). Before 1982, F. seoulensis failed to drawmedical attention. In 1982, a human sufferingfrom acute abdominal pain and fever (Seo et ai,1982) had eaten raw snake 7 days prior toadmission to the hospital. Later, the snakes,Rhabdophis (= Natrix) tigrina, were found tocarry metacercariae (Hong et ai, 1982). Twenty-five additional human infections were foundamong soldiers eating snakes during survivaltraining (Hong et al, 1984; 1986).

Life cycle studies revealed that the first inter-mediate host is a fresh water snail, Hippeutiscantori, and the second intermediate hosts aretadpoles and frogs (Seo et ai, 1988). The terrestrialsnake, R. tigrina, is regarded as a paratenic host.Mice, rats, Guinea pigs, and chicks were sus-ceptible to experimental infection (Seo, 1990).In experimental animals, the duodenum is themost favorite site of the worms, and villousatrophy and crypt hyperplasia are the two majorhistopathological features of the mucosa (Lee etai, 1985).

The diagnosis of fibricoliasis is based uponrecovery of eggs; however, the eggs should bedifferentiated from those of Echinostomatidae orFasciolidae. Treatment is successful with a singledose of praziquantel, 10-20 mglkg (Hong et ai,1984).

FAMIL Y ECHINOSTOMATIDAE

Echinostoma hortense Asada, 1926

This species was first described by Asada(1926) from the small intestine of house rats inJapan. The presence of E. hortense in Koreawas reported by Park (1938) from rats in Seouland human infection was reported by Seo et al(1983). A total of 77 egg or worm-proven caseswere reported (Lee et al, 1988b). Cheongsong-gun, an island area in the southeastern part ofKorea, was found to be highly endemic forhuman echinostomiasis, with an infection rate of22.4% in the villagers (Lee et al, 1988b).

The first intermediate hosts in Korea are freshwater snails, such as Lymnaea pervia and Radixauricularia coreana (Ahn and Kang, 1988). Fish


hosts are Misgurnus anguillicaudatus (Chai et ai,1985a), M. mizolepis, Odontobutis obsura inter-rupta, Morocco oxycephalus, Squalidus coreanus(Lee et ai, 1988b). Rats and dogs are natural finalhosts (Cho et ai, 1984).

Echinostoma cinetorchis Ando and Ozaki, 1923

This species was described by Ando and Ozaki(1923) from rats in Japan, and has been reportedfrom rats in Korea (Seo et al, 1964). Humaninfections are reported from Japan (Kawaharaand Yamamoto, 1933); four cases have beenreported from Korea (Seo et ai, 1980a; Ryang etai, 1986; Lee et ai, 1988a).

Life cycle studies in Korea (Seo et al, 1984c;Lee et al, 1990) showed that Hippeutis cantori, afresh water snail, can serve as the first as well asthe second intermediate host. Other fresh watersnails, such as Radix auricularia coreanus, Physaacuta, and Cipangopa/udina sp., or fresh waterfish, such as Misgurnus anguillicaudatus cancarry the metacercarial stage. Rats and dogswere found to be a natural final host (Cho et ai,1984). Albino rats were highly susceptible toexperimental infection with this fluke.

Echinochasmus japonicus Tanabe, 1926

This species was first described by Tanabe(1926) from the small intestine of experimentallyinfected dogs, cats, rats, mice, and birds withmetacercariae from fresh water fish. Recently,natural human infections were reported in Korea(Seo et ai, 1985).

The existence of this fluke in Korea wassuggested when metacercariae were found infresh water fish (Chun, 1964; Lee et ai, 1984a,b), and later the successful recovery of adultworms from experimental mice was reportedby Chai et al (1985c). The first intermediatehost in Korea is Parafossarulus manchouricus(Lee et ai, 1984a, b), and 18 species of freshwater fish, including Pseudorasbora parva,Hypomesus olidus and Gnathopogon strigatus(Lee et ai, 1984a, b) are second intermediatehosts. Natural infections are reported inchickens (unpublished) and ducks (Eom andRim, 1984).

FAMIL Y PLAGIORCHIIDAE

Plagiorchis sp.

Three specimens of Plagiorchis sp. were re-covered from a man after treatment with prazi-quantel (Hong et al, 1989a). The patient recalledeating raw fresh water fish. The specific diagnosisof worms has been made.

REFERENCES

Ahn YK. Lateolaborax japonicus, a role of the secondintermediate host of Metagonimus yokogawai.New MedJ 1983; 26:135-9.

Ahn YK, Kang HS. Development and cercarial shedd-ing of Echinostoma hortense in the snail host,Radixauriculariacoreana. JWonjuMedColl1988;1:137-52.

Ahn YK, Ryang VS. Epidemiological studies onMetagonimus infection along the Hongcheonriver, Kangwon Province. Korean J Parasitol1988; 26:207-13.

Ando R, Ozaki Y. On four new species of trematodesof the family Echinostomidae. DobutsugakuZasshi 1923; 35:108-19.

Asada 1. On a new echinostomatid trematode and itslife history. Trans Jpn Path Soc 1926; 16:293-4.

Chai JY. Study on Metagonimus yokogawai (Katsu-rada, 1912) in Korea. V. Intestinal pathology inexperimentally infected albino rats. Seoul J Med1979; 20: 104-17.

Chai JY, Cho SY, Seo BS. Study on Metagonimusyokogawai (Katsurada, 1912) in Korea. Korean JParasitoI1977; 15:115-20.

Chai JY, Hong SI, Lee SH, Seo BS. Stictodora sp.(Trematoda: Heterophyidae) recovered from aman in Korea. Korean J Parasitol1988; 26:127-32.

Chai IY, Hong SI, Sohn WM, Lee Sa, Seo BS.Studies on intestinal trematodes in Korea. XVI.Infection status of loaches with the metacercariaeof Echinostoma hortense. Korean J Parasit 1985a; 23:18-23.

Chai lY, Hong SI, Sohn WM, Lee SH, Seo BS.Further cases of human Heterophyes heterophyesnocens infection in Korea. Seoul J Med 1985b; 26:197-200.

Chai rv, Hong SI, Son DW, Lee SH, Seo BS.Metacercariae of the Echinochasmus japonicus

167


encysted in a fresh water fish, Pseudorasboraparva, and their development in experimentalmice. Korean JParasitol1985c; 23:221-9.

Chai lY, Seo BS, Lee SH. Studies on intestinal tre-matodes in Korea. XI. Two cases of human-infection by Heterophyes heterophyes nocens.Korean JParasitol1984a; 22:37-42.

Chai lY, Seo BS, Lee SH. Study on Metagonimusyokogawai (Katsurada, 1912) in Korea. VII.Susceptibility of various strains of mice toMetagonimus infection and effect of prednisolone.Korean J Parasitol1984b: 22: 153-60.

Chai lY, Seo BS, Lee SH, Hong ST. Growth anddevelopment of Pygidiopsis summa in rats andmice with a supplementary note on its morpho-logical characters. Korean JParasitol1986; 24:55-62.

Chai JY, Sohn WM. Identification of Stellantchasmusfalcatus metacercariae encysted in mullets inKorea. Korean J Parasitol1988; 26:65-8.

Chai lY, Yu lR, Lee SH, lung HC, Song IS, Cho SY.An egg-negative patient of acute metagonimiasisdiagnosed serologically by ELISA. Seoul J Med1989; 30: 139-42.

Choi DW, Lee JT, Hwang HK, Shin YD. Studies onthe larval trematodes from brackish water fishes.2. Observation on Metagonimus yokogawaiKatsurada, 1912. Korean JParasitol1966; 4:33-7.

Cho SY, Kang SY, Lee lB. Metagonimiasis inKorea. Session V: Intestinal fluke and Schisto-somajaponicum. Arzneim-Forsch/Drug Res 1984;34:1211-3.

Cho SY, Kim SI. Plecoglossus altivelis as a new fishintermediate host of Heterophyopsis continua.Korean JParasitol1985; 23: 173-4.

Chun SK. A study on the metacercaria of Metagonimustakahashii and Exorchis oviformis from Carassiuscarassius. Bull Pusan Fish Coli 1960a; 3:31-9.

Chun SK. A study on some trematodes whose inter-mediate hosts are brackish water fish. (I). Thelife history of Heterophyes continua the inter-mediate host of which is Lateolabrax japonicus.Bull Pusan Fish Coli 1960b; 3:40-4.

Chun SK. A study on some trematodes whose inter-mediate hosts are brackish water fish. (11). Thelife history of Pygidiopsis summa, the intermediatehost of which is Mugil cephalus. Bull Pusan FishColi 1963; 5:1-5.

Chun SK. Studies on the experiment of mode ofinfection of Clonorchis sinensis. 1. Bull PusanFish Coli 1964; 6:1-14.

168

Eom KS, Rim HI. A study on the parasitic helminthsof domestic duck (Anas platyrhynchos var.domestica Linnaeus) in Korea. Korean JParasitol1984; 22:215-21.

Eom KS, Son SY, Lee IS, Rim HI. Heterophyidtrematodes (Heterophyopsis continua, Pygidiopsissumma and Heterophyes heterophyes nocens)from domestic cats in Korea. Korean J Parasitol1985; 23: 197-202.

Hong SI, Choi IH, Seo BS. A human case of Pla-giorchis sp. Korean JParasit 1989a; 27:155.

Hong SI, Han IH. Two human infections by Hetero-phyopsis continua and Stictodora sp. Korean JParasitol1989; 27:344.

Hong SI, Lee SH, Chai lY, Seo BS. Recovery rate,growth and development of Heterophyopsis con-tinua in experimental chicks. Korean J Parasitol1990; 28:53-62.

Hong SJ, Seo BS, Lee SH, Chai JY. A human caseof Centrocestus armatus infection in Korea.Korean JParasito/1988; 26:55-60.

Hong SI, Woo He, Kim IT. Study on Centrocestusarmatus in Korea. I. Infection status of Zaccoplatypus and Z. temminckii with the metacercariaeof'C armatus. Korean JParasito/1989b; 27:41-6.

Hong ST, Chai lY, Lee SH. Ten human cases ofFibricola seoulensis infection and mixed onewith Stellantchasmus and Metagonimus. KoreanJParasito/1986; 24:94-6.

Hong ST, Cho TK, Hong SI, Chai rv, Lee SH, SeoBS. Fifteen cases of Fibricola seoulensis infectionin Korea. Korean JParasito/1984; 22:61-5.

Hong ST, Hong SJ, Lee SH, Seo BS, Chi IG. Studieson intestinal trematodes in Korea. VI. On themetacercaria and the second intermediate hostof Fibricola seoulensis. Korean J Parasito/1982;20:101-11.

Kang SY, Cho SY, Chai JY, Lee JB, Jang OH. A studyon intestinal lesions of experimentally reinfecteddogs with Metagonimus yokogawai. Korean JParasitol 1983; 21:53-73.

Kawahara S, Yamamoto E. Human cases of Echinostomacinetorchis. Tokyo Iji Shinshi 1933; 2840:11794.

Lee JK, Lee HI, Baek BK, Kim PG. Survey onencysted cercariae of trematodes from fresh-water fishes in Mangyeong riverside area. KoreanJ Parasitol1984a; 21:187-92.

Lee JK, Lee HI, Baek BK, Kim PG. Survey onencysted cercariae of trematodes from fresh-water fishes in Tongjin riverside area. Korean


J Parasitol 1984b; 22:190-202.

Lee SH, Chai lY, Hong ST, Sohn WM. Experimentallife history of Echinostoma cinetorchis. Korean JParasitol 1990; 28:39-44.

Lee SH, Yoo BH, Hong ST, Chai lY, Seo BS, ChiIG. A histopathological study on the intestineof mice and rats experimentally infected byFibricola seoulensis. Korean J Parasitol 1985;23:58-72.

Lee SK, Chung NS, Ko IH, Ko HI, Sohn WM. A caseof natural human infection by Echinostomacinetorchis. Korean J Parasitol 1988a; 26:61-4.

Lee SK, Chung NS, Ko IH, et al. An epidemiologicalsurvey of Echinostoma hortense infection inChongsong-gun, Kyongbuk Province. Korean JParasitol 1988b; 26:199-206.

Miyamoto K, Nakao M, Inaoka T. Studies on thezoonoses in Hokkaido, Japan. 5. On the epide-miological survey of Echinostoma hortense Asada,1926. Jpn J Parasitol1983; 32:261-9.

Noda K. The larval development of Stellantchasmusfalcatus (Trematoda: Heterophyidae) in the firstintermediate host. J Parasitol 1959; 45:635-42.

Park IT. A rat trematode, Echinostoma hortense Asada,from Korea. Keijo J Med 1938; 9:283-6.

Rim HI, Chu OS, Lee IS, 100 KH, Won CV.Anthelmintic effects of various drugs againstmetagonimiasis. Korean J Parasitol 1987; 16:117-22.

Ryang VS, Ahn YK, Kim WT, Shin KC, Lee KW,Kim TS. Two cases of human infection byEchinostoma cinetorchis. Korean J Parasitol 1986;24:71-6.

Saito S. On the validity of Metagonimus spp. Proc ofJap Parasite Taxon Morphol Conf 1984; 2:1-6(in Jpn),

Seo BS. Fibricola seoulensis Seo, Rim and Lee, 1964(Trematoda) and fibricoliasis in man. Seoul J

Med 1990; 31:6/-96.

Seo BS, Cheong SK, Chai lY, Lee SH, Lee lB.Histopathology of small intestine of rats and miceexperimentally infected with Pygidiopsis summa.SeoulJ Med 1986; 27:125-34.

Seo BS, Cho SY, Chai lY. Studies on intestinaltrematodes in Korea. I. A human case ofEchinostoma cinetorchis infection with an epide-miological investigation. Seoul J Med 1980a; 21:21-9.

Seo BS, Cho SY, Chai IY, Hong ST. Studies onintestinal trematodes in Korea. II. Identification

of the metacercariae of Heterophyes heterophyesnocens in mullets of three southern coastalareas. Seoul J Med 1980b; 21 :30-8.

Seo BS, Hong ST, Chai lY. Studies on intestinaltrematodes in Korea. Ill. Natural humaninfection of Pygidiopsis summa and Heterophyesheterophyes nocens. Seoul J Med 1981a; 22:228-35.

Seo BS, Hong ST, Chai lY, Cho SY. Studies onintestinal trematodes in Korea. IV. Geographicaldistribution of Pygidiopsis and Heterophyesmetacercariae. Seoul J Med 198/ b; 22:236-42.

Seo BS, Hong ST, Chai lY, Lee SH. Studies onintestinal trematodes in Korea. VII. A humancase of Echinostoma hortense infection. KoreanJ Parasitol1983; 21:219-23.

Seo BS, Lee SH, Chai lY, Hong SI. Studies onintestinal trematodes in Korea. XII. Two cases ofhuman infection by Stellantchasmus falcatus.Korean J Parasito/1984a; 22:43-50.

Seo BS, Lee SH, Chai IY, Hong SI. Studies onintestinal trematodes in Korea. XIII. Two casesof natural human infection by Heterophyopsiscontinua and the status of metacercarial infectionin brackish water fishes. Korean J Parasitol 1984.b; 22:51-60.

Seo BS, Lee SH, Chai lY, Hong SI. Studies onintestinal trematodes in Korea. XX. Four casesof natural human infection by Echinochasmusjaponicus. Korean J Parasitol 1985; 23:214-20.

Seo BS, Lee SH, Chai JY, Hong SI, Hong ST. Thelife cycle and larval development of Fibricolaseoulensis (Trematoda: Diplostomatidae). KoreanJ Parasitol 1988; 26:179-88.

Seo BS, Lee SH, Cho SY, et al. An epidemiologicstudy on clonorchiasis and metagonimiasis inriverside areas in Korea. Korean J Parasitol 1981c; 19:137-50.

Seo BS, Lee SH, Hong ST, Hong SI, Kim CV, LeeHY. Studies on intestinal trematodes in Korea.V. A human case infected by Fibricola seoulensis(Trematoda: Diplostomatidae), Korean J Parasitol1982; 20:93-9.

Seo BS, Park YH, Chai lY, Hong SJ, Lee SH.Studies on intestinal trematodes in Korea. XIV.Infection status of loaches with metacercariae ofEchinostoma cinetorchis and their developmentin albino rats. Korean J ParasitoI1984c; 22:181-9.

Seo BS, Rim HJ, Lee CW. Studies on the parasitichelminths of Korea. I. Trematodes of rodents.Korean J Parasitol 1964; 2:2<ki.

169


Seo BS, Rim HJ, Lee SH, et al. Two cases of metago-nimiasis with special reference on the egg layingcapacity in the human host. Seoul J Med 1971'12:234-41. '

Sohn WM, Chai N, Lee SH. Two cases of naturalhuman infection by Heterophyes nocens and theinfection status of heterophyid metacercariae inmullets from Samcheonpo, Kyongnam Province.Inje Med J 1989; 10:443-52.

Takahashi S. A contribution to the life-history ofStamnosoma armatum Tanabe. Okayama Igakkai

Zasshi 1929; 4:1759-71.

Tanabe H. Studien uber die Trematoden mit Susswasser-fischen als Zwischenwirt. 1.Stamnosoma armatumn.g., n.sp. Kyoto Igaku Zasshi 1922; 19:239-52.

Tanabe H. Studies on trematodes with fresh waterfishes as their intermediate host. Ill. On a newspecies, Echinochasmus japonicus (n. sp.) NipponByori Gakkai Kaishi 1926; 16:295-6.

170

intestinal trematodes infecting humans in korea

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