Infection Status with Clonorchis sinensis Metacercariae in Fish from Tamjin-gang (River) in Jeollanam-do, Republic of Korea

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1 ISSN (Print) ISSN (Online) ORIGINAL ARTICLE Korean J Parasitol Vol. 56, No. 2: 888, April 8 Infection Status with Clonorchis sinensis Metacercariae in Fish from Tamjingang (River) in Jeollanamdo, Republic of Korea KiBok Yoon, HyunCheol Lim, Doo Young Jeon, Sook Park, ShinHyeong Cho 2, JungWon Ju 2, SungShik Shin, ByoungKuk Na 4, WoonMok Sohn 4, * Division of Microbiology, Jeollanamdo Institute of Health and Environment, Muan 58568, Korea; 2 Division of Vectors and Parasitic Diseases, Centers for Disease Control and Prevention, Osong 2859, Korea; Department of Parasitology, College of Veterinary Medicine, Chonnam National University, Gwangju 686, Korea; 4 Department of Parasitology and Tropical Medicine, and Institute of Health Sciences, Gyeongsang National University College of Medicine, Jinju 52727, Korea Abstract: The present study was performed to investigate the infection status with Clonorchis sinensis metacercariae (CsMc) in es from 2 sites, the middle and lower reaches, of Tamjingang (River) in Jeollanamdo, the Republic of Korea. Total,2 es in 22 species were collected from the middle reaches in Jangheunggun for 4 years (47) and 57 es in 7 species were also collected from the lower reaches in Gangjingun in 4 and 7. They were all individually with the artificial digestion method in our laboratory. CsMc were in 22 (28.5%) out of,2 es from Jangheunggun, and in 6 (.%) out of 57 es from Gangjingun, and their densities were 5 and 57 per each. In the species with CsMc, positive rates were 6.5% in Jangheunggun and 62.7% in Gangjingun. A total of 222 were and they were all with CsMc. The average intensity was 0 CsMc in the index, P. herzi (95 in Jangheunggun and 2 in Gangjingun). In P. herzi bimonthly in 7, the intensity was commonly most higher in March in 2 surveyed sites, however the significant seasonal endemicity was not showed. Conclusively, it was confirmed that CsMc is more or less prevalent in es from Tamjingang and their endemicity is higher in from the lower reaches in Gangjingun than the middle reaches in Jangheunggun in Jeollanamdo, Korea. Key words: Clonorchis sinensis, metacercaria, freshwater, index,, Tamjingang INTRODUCTION Received 9 February 8, revised March 8, accepted 0 April 8. * Corresponding author (wmsohn@gnu.ac.kr) 8, Korean Society for Parasitology and Tropical Medicine This is an Open Access article distributed under the terms of the Creative Commons Attribution NonCommercial License ( which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original work is properly cited. In the nationwide survey on the helminthic infection in the Republic of Korea (Korea), the prevalence of clonorchiasis, Clonorchis sinensis infection, was.86%, 92,540 residents with this endemic disease estimated. Nowadays, it is the highest value among the prevalences of parasitic diseases in Korea []. The prevalence of this endemic disease has maintained at relatively high levels in residents of riverside areas in Korea [2 6]. Especially, Cho et al. [5] reported the egg positive rates of C. sinensis in residents living in the 4 river basins, Nakdonggang (gang means River), Seomjingang, Yeongsangang and Geumgang, located in southern part of Korea. Recently, Jeong et al. [6] reported the prevalences of clonorchiasis in the adjacent residents of 5 major rivers, i.e., Nakdonggang, Seomjingang, Geumgang, Yeongsangang and Hangang. However, the endemicity of this trematode infections is rarely reported in the riverside residents of Tamjingang except for the Seo et al. [2] performed in 98. Many Korean parasitologists freshwater es, the infection source of clonorchiasis, from various endemic areas to estimate the endemicities of liver fluke infections [76]. Especially, in 08, Kim et al. [0] widely surveyed freshwater es from 4 localities to know the infection status with Clonorchis sinensis metacercariae (CsMc) in Korea. Cho et al. [2] investigated the infection status of CsMc in freshwater from wide regions, which tentatively divided by the latitudinal levels of Korean peninsula in. Cho et al. [] also surveyed on the prevalence of zoonotic trematode metacercariae in freshwater from Gangwondo (do=province), Korea. 8

2 84 Korean J Parasitol Vol. 56, No. 2: 888, April 8 Sohn et al. [4] investigated the infection status of digenetic trematode metacercariae including C. sinensis in freshwater from the water systems of Hantangang and Imjingang located in relatively northern regions of Korea. Recently, Sohn et al. [5] surveyed the prevalence of CsMc in freshwater es from the water systems of Seomjingang. Sohn et al. [6] also reported the infection tendency of CsMc by the subfamily groups in Cyprinidae hosts from a highly endemic site, Wicheon (a branch of Nakdonggang), in Gunwigun, Gyeongsangbukdo, Korea. Tamjingang is one of the major rivers in Jeollanamdo together with Seomjingang and Yeongsangang. It rises from a mountinous area between Yuchimyeon (myeon =township) in Jangheunggun (gun=county) and Geumjeongmyeon in Yeongamgun, flows via Jangheunggun and Gangjingun and flows into the South Sea in the Gangjin Bay, Jeollanamdo, Korea [7]. Its riverside areas have been known as the endemic area of intestinal fluke, Metagonimus yokogawai and heterophyid flukes [2,822]. However, the infection status with CsMc in from this river has not been widely and systematically yet. Therefore, we performed the present study to investigate the infection status with CsMc in from 2 local sites of Tamjingang in Korea. MATERIALS AND METHODS Fish collection Total,2 es in 22 species were collected in the middle reaches of Tamjingang (River) in Jangheunggun (Latitude: ; Longitude: ), Jeollanamdo, Korea for 4 years (47). Total 57 es in 7 species were also collected in the lower reaches of Tamjingang in Gangjingun (Latitude: 4.805; Longitude: ), Jeollanamdo in 204 and 7. Table. Infection status of Clonorchis sinensis metacercariae in es from the middle reaches of Tamjingang (River) in Jangheunggun, Jeollanamdo Year and sp. 4 Hemiculter eigenmanni Coreoperca herzi Sarcocheilichthys nigripinnis 5 Odontobutis platycephala Acheilognathus yamatsutae Squalidus gracilis majimae Sarcocheilichthys nigripinnis 6 Zacco platypus Sarcocheilichthys nigripinnis Acanthorhodeus gracilis 7 Sarcocheilichthys nigripinis Acheilognathus koreensis Acanthorhodeus gracilis (8.0) 9 (95.0) 4 (00) 4 (66.7) (.) (00) 4 (59.4) 5 (00) 2 (0.0) 4 (00) (8.) 2 (22.2) 4 (80.0) 2 (50.0) 2 (66.7) 2 (66.7) 64 (6) 6 (00) 2 (6.7) (.5) 2 (7.4) 8 (8.) 5 (88.2) 5 (00) 9 (00) 88 (47.8) 7 (5.) 9 (6.0) 22 (95.7) 8 (80.0) 2 (40.0) (00) (00) 29 (77.7) CsMc Total (6.5) Fishes collected from the middle reaches of Tamjingang in Jangheunggun Total es in species were in 4. Fish species (no. of ) were Zacco temminckii (0), Carassius auratus (25), Zacco platypus (), Acheilognathus yamatsutae (), Odontobutis platycephala (6), Micropterus salmoides (5), Acanthorhodeus gracilis () including 6 ones with CsMc in Table. Total 24 es in 5 species were in 5. Fish species (no. of ) were Z. temminckii (2), C. auratus (0), Z. platypus (27), Coreoperca kawamebari (27), Plecoglossus altivelis (8), Acheilognathus koreensis (4) including 9 ones with CsMc in Table. Total 02 es in 6 species were in 6. Fish species (no. of ) were Z. temminckii (28), C. kawamebari (24), P. altivelis (22), C. auratus (), O. platycephala (2), Siniperca scherzeri (6), C. herzi () and M. salmoides () including 8 ones with CsMc in Table. Total 4 es in 8 species were in 7. Fish species (no. of ) were Z. temminckii (62), Z. platypus (6), C. auratus (4),

3 Yoon et al.: Clonorchis sinensis metacercariae in from Tamjingang 85 Table 2. Infection status of Clonorchis sinensis metacercariae in from the middle reaches of Tamjingang (River) in Jangheunggun, Jeollanamdo Year CsMc (00) (00) (00) March May July October (00) (00) (00) 2 (00) Total (00) C. kawamebari (), O. platycephala (8), P. altivelis (2), P. esocinus (2), C. herzi (0), A. yamatsutae () and Cyprinus carpio (2), including 8 ones with CsMc in Table. Fishes collected from the lower reaches of Tamjingang in Gangjingun Total 0 in 2 species were in 4. Fish species (no. of ) were Z. platypus (), C. auratus (9), Z. temminckii (5), Lateolabrax japonicus (2), O. platycephala () and Mugil cephalus () including 6 ones with CsMc in Table. Total 407 es in 4 species were in 7. Fish species (no. of ) were Z. platypus (55), C. auratus (4), P. altivelis (40), C. kawamebari (25), O. platycephala (25), Z. temminckii (2) and C. herzi (), including 7 ones with CsMc in Table. Examination methods All collected es with ice were transferred to the laboratory of the Department of Parasitology and Tropical Medicine, Gyeongsang National University College of Medicine, Jinju, Korea. After the identification of species, they were individually ground with a mortar or grinder. Each ground meat was mixed with artificial gastric juice and the mixture was incubated at 6 C for 2 hr. The digested material was filtered with mm of mesh, and washed with 0.85% saline until the supernatant is clear. The sediment was carefully under a stereomicroscope. CsMc were separately collected by the general feature [], and they were counted to get hold of infection rates (%) and densities ( CsMc per ) by species. Table. Infection status of Clonorchis sinensis metacercariae in es from the lower reaches of Tamjingang (River) in Gangjingun, Jeollanamdo Year and sp. 4 Acanthorhodeus macropterus 7 Sarcocheilichthys nigripinis RESULTS 8 (28.6) 4 (.0) (7.5) (00) 2 (00) (00) 2 (.9) (00) (.2) 2 (50.0) 8 (00) (2.4) 6 (75.0) 40 (7.8) CsMc Total (62.7) Infection status of with CsMc in middle reaches of Tamjingang The metacercariae of C. sinensis (CsMc) were in 22 (6.5%) out of 524 es in 6 species from the middle reaches of Tamjingang in Jangheunggun, Jeollanamdo, and their average density was 5 per. In the positive species with CsMc, prevalences were 59.4%, 6%, 47.8%, and 77.7% from 4 to 7 and their densities were 69, 42, 82 and 28 per respectively. The infection status with CsMc by the species and surveyed years was detailedly shown in Table. All 52 striped shinner, P. herzi, were with CsMc, of which intensities were 86, 66, 8, and 45 in average from 4 to 7. In case of this species in 7, intensities with CsMc were in March, 2 in May, 0 in July and 25 in October respectively (Table 2). Infection status of with CsMc in lower reaches of Tamjingang The CsMc were in 6 (62.7%) out of 257 es in 8 species from the lower reaches of Tamjingang in Gangjingun, Jeollanamdo, and their average density was 57 per. In the positive species, prevalences were.9%

4 86 Korean J Parasitol Vol. 56, No. 2: 888, April 8 in 4 and 7.8% in 7 and their densities were 9 and 60 CsMc per. The infection status with CsMc by the species and surveyed years was detailedly revealed in Table. All 70 striped shinner, P. herzi, were with CsMc, of which intensities were 242 and 5 in average in 4 and 7. In case of this species in 7, intensities with CsMc were 95 in March, 64 in May, 59 in July and 6 in October respectively (Table 4). Comparison of the infection status of with CsMc in 2 surveyed sites of Tamjingang Total,649 es were in this study. Among them,,2 (68.7%) were caught from the middle reaches of Tamjingang in Jangheunggun and remain 57 (.4%) were from the lower reaches in Gangjingun, Jeollanamdo. The overall positive rate with CsMc was 29.% in,649 es from Tamjingang. That was 28.5% in,2 es from Jangheunggun and was.% in 57 es from Gangjingun. A total of 222 P. herzi were and they were all with CsMc. The average density was 0 CsMc in the index, P. herzi (95 in Jangheunggun and 2 in Gangjingun) (Table 5). Table 4. Infection status of Clonorchis sinensis metacercariae in an index,, from the lower reaches of Tamjingang (River) in Gangjingun, Jeollanamdo Year CsMc 4 (00) March May July October 5 9 (00) 5 (00) 9 (00) (00) Total (00) DISCUSSION By the present study, it was confirmed that CsMc are more or less prevalent in from Tamjingang. Total positive rate, 29.%, and average metacercarial density, 5 per, were not so high (Table 5). However, the prevalence (00%) and metacercarial density (0) in the index, P. herzi, were shown the relatively higher level. In the positive species group, the endemicity of CsMc was slightly higher in from the lower reaches in Gangjingun (prevalence: 62.7%; density: 57) than in from the middle reaches in Jangheunggun (6.5%; 5). In P. herzi, the metacercarial density was higher in the lower reaches (2) than in the middle reaches (95). These findings suggested that the endemicity with CsMc is more or less higher in from the lower reaches in Gangjingun than in from the middle reaches in Jangheunggun, Jeollanamdo, Korea. Cho et al. [2] es from 2 sites, Gangjingun (58 in spp.) and Jangheunggun (52 in 9 spp.), of Tamjingang in 05. They 6 CsMc per in 9 (76.5%) out of 5 es (9 spp.) from Gangjingun, but they found no CsMc in 52 es from Jangheunggun. From these findings, we can speculate that the endemicity of CsMc has been highly maintained in from Gangjingun, however, no CsMc in from Jangheunggun unlike in this study is questionable. Two species, P. herzi and S. variegatus wakiye, were showed to be the highly susceptible hosts of C. sinensis in Cho et al. [2]. Their susceptibility index of CsMc, 4 in P. herzi and 56 in S. variegatus wakiye, were very high, when we compared with those of present study, 0 in P. herzi. On the other hand, Sohn et al. [6] reported that the susceptibility index of CsMc is,0 in 2 gobioninid es, i.e., 69 P. herzi, 7 Squalidus spp., 25 S. variegatus wakiye, and 2 Pseudorasbora parva, from Wicheon in Gunwigun, Gyeongsangbukdo. Kim et al. [0] reported 8 CsMc in average densi Table 5. Comparison of the infection status a with C. sinensis metacercariae in from 2 regions of Tamjingang (River) Items Infection status of C. sinensis metacercariae in from Jangheunggun Gangjingun Total,2 (68.7) 57 (.4),649 (00) Overall positive rate (%) 22/,2 (28.5) 6/57 (.) 48/,649 (29.) Total metacercarial density No. (%) b of P. herzi 52 (.4) 70 (.5) 222 (.5) Metacercarial density in P. herzi a Positive rate: / 00; metacercarial density: mean no. of CsMc per. b P. herzi/total 00.

5 Yoon et al.: Clonorchis sinensis metacercariae in from Tamjingang 87 ty in 0 P. herzi, from Yangcheon in Sancheonggun, Gyeongsangnamdo. In the metacercarial surveys for the epidemiology of zoonotic trematode infections, the sampling of is one of the important factors to obtain the more precise information. Total,649 es were collected from 2 sites (,2 from the middle reaches in Jangheunggun and 57 from the lower reaches in Gangjingun, Jeollanamdo) of Tamjingang in this study. In the middle reaches, total,2 es in 22 species were for 4 years (47) and a total of 57 es in 7 species from the lower reaches were in 4 and 7. The difference of number in 2 surveyed areas is depends upon the number of years. The striped shinner, P. herzi (222:.5%), was the most dominant species, and followed by pale chub, Z. platypus (2: 2.9%), dark chub, Z. temminckii (78: 0.8%), crusian carp, C. auratus (78: 0.8%), and goby minnow, P. esocinus (7: 8.%) among the species in this study. The numbers of striped shinner in each 2 reaches were 52 (middle:.4%) and 70 (lower:.5%). Those of pale chub were 8 (2.2%) and 75 (4.5%), and of crusian carp were 6 (0.%) and 62 (2.0%). According to the above findings, major 4 species were collected in similar proportions in 2 surveyed areas. However, the dark chub, Z. temminckii, was collected more in the middle (52:.4%) than in the lower reaches (26: 5.0%). Total 5 species (in 6 genera 9 families) have been reported as the second intermediate hosts of C. sinensis in Korea [76]. In the present study, CsMc were in 6 species, i.e., Acanthorhodeus gracilis, A. macropterus, Acheilognathus lanceolatus, A. koreensis, A. rhombeus, A. yamatsutae, Coreoperca herzi,, Hemiculter eigenmanni, Odontobutis platycephala,,, Sarcocheilichthys nigripinnis morii, S. variegatus wakiye, Squalidus gracilis majimae, and Zacco platypus. They all had been listed as the second intermediate hosts of C. sinensis in Korea [96]. According to the recent studies, CsMc were found in es from the water system of Imjingang and Hantangang located in the northern part of Korea, although their prevalences and densities were very low [4]. Whereas CsMc were not at all in es from the water systems of Hangang in Gangwondo []. In es from Geumgang, the prevalence and density of CsMc were also revealed in a low level [2]. They were showed in the moderate level in es from Yeongsangang and Seomjingang in Jeollanamdo [2,5] like those in this study. However, es from localities, i.e., Wicheon (in Gunwigun, Gyeongsangbukdo), Banbyeoncheon (in Yeongyanggun, Gyeongsangbukdo) and Yangcheon (in Sancheonggun, Gyeongsangnamdo), of Nakdonggang were highly and heavily with CsMc [2,6]. Some species of freshwater edible in raw practically act as the infection source of clonorchiasis in Korea. Among 22 species in this study, 5 ones, i.e., crusian carp (C. auratus), Korean and Japanese aucha perch (C. herzi and C. kawamebari), sweet smelt (Plecoglossus altivelis), and Korean dark sleeper (O. platycephala), are frequently eaten in raw in Korea. A total of 472 (28.6%) edible in raw, i.e., 78 crusian carp, 9 Korean and 09 Japanese aucha perch, 92 sweet smelt and 74 Korean dark sleeper, were in this study, but only 2 (0.4%), C. herzi and O. platycephala, were with only CsMc of each. In even such a highly endemic area, Wicheon, total (8.8%) out of 4 C. auratus were with total CsMc, 2 (.%) C. herzi were retained with 4 CsMc and only (.%) S. scherzeri were with total 6 CsMc, respectively [6]. No CsMc were in 4 species, i.e., C. herzi (57), C. auratus (42), S. scherzeri (), and C. carpio (2), from Seomjingang [5]. Fortunately, these species edible in raw are less prevalent with CsMc in Korea. Then, what kinds of factors are acted in maintenance of the endemicity of clonorchiasis in Korea? The chopping board contaminated with meat may be act as the other transmission route of clonorchiasis in the riverside endemic areas of Korea. Conclusively, it is confirmed that the endemicity of CsMc is moderately high in es from Tamjingang, which is known to be the endemic area of heterophyid flukes, including Metagonimus yokogawai and Heterophyes nocens [2,822]. The surveillances on the zoonotic borne trematode infections should be constantly done in this river basin. ACKNOWLEDGMENTS This study was supported by an anticommunicable diseases control program, 4E54000 (Investigation of borne parasites and acquisition of their biological resources in the southern regions of Korea) of National Institute of Health (NIH), Korea Centers for Disease Control and Prevention (KCDCP). We thank JungA Kim and HeeJoo Kim (Department of Parasitology and Tropical Medicine, Gyeongsang National University College of Medicine, Jinju, Korea), for their

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