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Heterophyid Metacercarial Infections in Brackish Water Fishes from Jinju-Man (Bay), Kyongsangnam-Do, Korea

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Heterophyid Metacercarial Infections in Brackish Water Fishes from Jinju-Man (Bay), Kyongsangnam-Do, Korea Korean Journal of Parasitology Vol. 44, No. 1: 7-13, March 2006 Heterophyid metacercarial infections in brackish water fishes from Jinju-man (Bay), Kyongsangnam-do, Korea Do Gyun KIM1), Tong-Soo KIM2), Shin-Hyeong CHO2), Hyeon-Je SONG3) and Woon-Mok SOHN4)* 1)Department of Obstetrics and Gynecology, Dongguk University College of Medicine, Gyeongju 780-350, 2)Department of Parasitology, National Institute of Health, Seoul 122-701, 3)Microbiology Division, Jeollanam-do Institute of Health and Environment, Gwangju 502-810, 4)Department of Parasitology and Institute of Health Sciences, Gyeongsang National University College of Medicine, Jinju 660-751, Korea Abstract: Heterophyid metacercarial infections in brackish water fishes, i.e., perch, shad, mullet, redlip mullet, and goby, of Jinju-man (Bay), Kyongsangnam-do, Korea, were investigated using a digestion technique. Among 45 perch (Lateolabrax japonicus), the metacercariae of Heterophyopsis continua were found in 55.6% (18.5 metacercariae per fish), Stictodora spp. in 28.9% (3.6), and Metagonimus takahashii in 6.7% (17.0). The metacercariae of H. continua were detected in 23 (65.7%) of 35 shad (Konosirus punctatus). Among 15 mullet (Mugil cephalus), the metacercariae of Pygidiopsis summa were found in 100% (105.9 metacercariae per fish), Heterophyes nocens in 40.0% (8.5), H. continua in 13.3%, and Stictodora spp. in 6.7%. Among 12 redlip mullet (Chelon haematocheilus), the metacercariae of P. summa were detected in 91.7% (1,299 metacercariae per fish), H. nocens in 16.7%, and Stictodora spp. in 16.7%. Among 35 gobies (Acanthogobius flavimanus), the metacercariae of Stictodora spp. were found in 82.9% (44.5 metacercariae per fish), and H. continua in 25.7% (2.8). The adult flukes recovered from a cat experimentally infected with metacercariae from perches were compatible with M. takahashii. The results confirm that the estuarine fish in Jinju-man (Bay) are heavily infected with heterophyid metacercariae. Furthermore, it was found for the first time that the perch acts as a second intermediate host for M. takahashii. Key words: Heterophyidae, metacercaria, Metagonimus takahashii, Heterophyes nocens, Heterophyopsis continua, Pygidiopsis summa, Stictodora sp., fish, Jinju-man (Bay), Korea Pygidiopsis, Procerovum, Haplorchis, and Stictodora, are INTRODUCTION known to be human-infecting heterophyid flukes About 30 species of 9 genera, i.e., Metagonimus, (Chai and Lee, 2002). During the 1970’s it was Heterophyes, Heterophyopsis, Stellantchasmus, Centrocestus, believed that Metagonimus yokogawai was the only human pathogenic fluke in Korea. However, since �Received 8 November 2005, accepted after revision 3 then, additional human pathogens, such as Heterophyes January 2006. nocens, Heterophyopsis continua, Stellantchasmus falcatus, �This work was supported by an Anti-Communicable Pygidiopsis summa, Centrocestus armatus, Metagonimus Diseases Control Program of the National Institute of Health takahashii, Metagonimus miyatai, Stictodora fuscata and (NIH 348-6111-215), Ministry of Health and Welfare, Republic of Korea. Stictodora lari have been added to the list of pathogen- *Corresponding author (e-mail: [email protected]) ic heterophyid flukes (Chai and Lee, 2002). 8 Korean J. Parasitol. Vol. 44, No. 1: 7-13, March 2006 Table 1. Estuarine fish species examined in this study Species of fish No. of fish Length (cm) Weight (g) (common name) examined Range Average Range Average Lateolabrax japonicus 45 13.0-20.0 15.7 27.1-101.5 58.9 (perch) Konosirus punctatus 35 11.5-18.0 15.8 21.7-114.7 76.3 (shad) Mugil cephalus 15 12.0-24.0 20.0 22.4-178.3 121.6 (mullet) Chelon haematocheilus 12 15.4-26.0 21.3 34.5-224.6 128.1 (redlip mullet) Acanthogobius flavimanus 35 11.2-20.8 15.3 22.4-84.8 47.8 (goby) Nevertheless, considerably earlier, trematodes of genus Heterophyes were suggested to have a national MATERIALS AND METHODS distribution and possibly infect man, after eggs were discovered in the human feces (Stryker, 1914; Between early September and late October of 2004, Imanishi, 1914), metacercariae in mullet (Asada, 1934), 45 perch (L. japonicus), 35 shad (K. punctatus), 15 mul- and worms from animal intestines (Kobayashi, 1925; let (M. cephalus), 12 redlip mullet (Chelon haema- Furuyama, 1930). tocheilus), and 35 gobies (A. flavimanus) were collected Heterophyid flukes can cause abdominal pain and from Jinju-man in Kyongsangnam-do. All collected diarrhea in infected humans, and their eggs, after fishes were transferred to our laboratory, measured being transferred by the blood stream, may produce for length and weight, and examined by artificial eosinophilic granuloma in the heart, brain, and spinal digestion method (Table 1). Trematode metacercariae cord (Africa et al., 1940; Kang et al., 1983; Cho et al., were segregated, collected under a stereomicroscope, 1985). In terms of sources of infection, several kinds of and categorized according to measurements and mor- brackish water fish, such as, perch (Lateolabrax japoni- phological characteristics. Intensities of infection and cus), shad (Konosirus punctatus), mullet (Mugil infection rates were then calculated. Metagonimus sp. cephalus), and goby (Acanthogobius flavimanus), have metacercariae were used to experimentally infect a cat been identified in Korea (Chun 1960, 1963; Seo et al., to obtain adult worms. Twenty-one days after infec- 1980, 1981, 1984; Chai and Sohn, 1988; Chai et al., tion, adult worms were recovered from the small 1989; Sohn et al., 1994; Sohn and Moon, 2001). These intestine, fixed with 10% neutral buffered formalin, fish are sometimes heavily infected with the metacer- and stained with Semichon’s acetocarmine in order to cariae of heterophyid flukes, and are popularly eaten study their morphological characteristics. raw by residents in coastal areas. However, no simul- taneous investigation has been conducted on the RESULTS infection status of heterophyid metacercariae in a range of estuarine fish species, in a particular area. Infection status of heterophyid metacercariae Therefore, the purpose of this study is to systematical- Metacercariae of H. continua, Stictodora spp. and M. ly investigate the infection status of heterophyid fluke takahashii were detected in the perch (Table 2). Total metacercariae in estuarine fish species caught in Jinju- 152 metacercariae of H. continua (1-40/fish) were man (Bay), which is located in the middle of southern detected in 23 (65.7%) of 35 shad. The metacercariae of coast of Korea. P. summa, H. nocens, H. continua and Stictodora sp. Kim et al.: Heterophyid metacercarial infections in fishes of Jinju Bay 9 Table 2. Infection status of heterophyid metacercariae in Table 4. Infection status of heterophyid metacercariae in the perch, Lateolabrax japonicus, from Jinju-man the redlip mullet, Chelon haematocheilus, from Jinju-man No. (%) No. of metacercariae No. (%) No. of metacercariae Fluke species of fish detected Fluke species of fish detected infected Total Range Average infected Total Range Average Heterophyopsis continua 25 (55.6) 463 1-81 18.5 Pygidiopsis summa 11 (91.7) 14,283 1-14,190 1,298.5 Stictodora spp. 13 (28.9) 347 1-8 33.6 Heterophyes nocens 02 (16.7) 4 1-3 2.0 Metagonimus takahashii 33 3(6.7) 351 1-49 17.0 Stictodora sp. 02 (16.7) 2 - 1.0 2.8 metacercariae (1-8/fish). Table 3. Infection status of heterophyid metacercariae in the mullet, Mugil cephalus, from Jinju-man Morphology of metacercariae and adults of No. of metacercariae No. (%) Metagonimus takahashii (Fig. 2) Fluke species of fish detected The disc shaped metacercariae of M. takahashii infected Total Range Average detected in the perch were 150-175 (mean 162) x 150- Pygidiopsis summa 15 (100) 1,588 1-980 105.9 163 (mean 156) µm in size. Their ventral suckers, devi- Heterophyes nocens 06 (40.0) 51 1-43 8.5 ated to one side and were larger than the oral sucker. Heterophyopsis continua 02 (13.3) 4 1-3 2.0 Brownish pigments were scattered over whole bodies Stictodora spp. 01 0(6.7) 21 - 21.0 and a black excretory bladder was located near the posterior end. Adults recovered from an experimental were detected in mullet (Table 3). In redlip mullet cat were 580-820 (mean 688) x 250-350 (mean 288) µm (Fig. 1), we detected the metacercariae of P. summa, H. in size, and had a sharp anterior and a round posteri- nocens and Stictodora sp. (Table 4), and in gobies, we or end. A round oral sucker (mean 39 x 53 µm) was detected the metacercariae of Stictodora spp. and H. located at the anterior end, followed by a muscular continua. In total, 1,291 metacercariae of Stictodora spp. pharynx (mean 31 x 24 µm), and a relatively long (1-194/fish) were collected from 29 gobies (82.9%). H. esophagus (mean 93 µm) and the intestine. The right continua metacercariae were from 9 gobies (27.7%), deviated ventral sucker (mean 77 x 49 µm) was locat- with an average infection density per infected fish of ed at the anterior 2/5 of worm. The oval-shaped ovary (mean 61 x 59 µm) was located in posterior 1/3- 1/2 median. The seminal vesicle (mean 65 x 147 µm) was long saccular, often divided into two parts by a constriction (mean 59 x 35 µm), and was transversely located in the left space between the ventral sucker and ovary. The seminal receptacle (mean 116 x 92 µm) was irregular in shape, and situated near the right side of the ovary. Two testes were arranged obliquely in tandem and apart from each other. The right testis (mean 159 x 88 µm) was located more posteriorly than the left testis (mean 135 x 92 µm). The uterus occupied all available space from the acetabular level to near Fig. 1. Mullet, Mugil cephalus (upper) and redlip mullet, posterior end of the body, and the uterine loop passed Chelon haematocheilus (lower).
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