Prevalence of <italic>Clonorchis sinensis</italic> Metacercariae in Freshwater Fish from Three Latitudinal Regions of the Korean Peninsula

Shin-Hyeong Cho; Woon-Mok Sohn; Byoung-Kuk Na; Tong-Soo Kim; Yoon Kong; Keeseon Eom; Won-Seok Seok; Taejoon Lee

doi:10.3347/kjp.2011.49.4.385

Korean J Parasito > Volume 49(4):2011 > Article

Cho, Sohn, Na, Kim, Kong, Eom, Seok, and Lee: Prevalence of Clonorchis sinensis Metacercariae in Freshwater Fish from Three Latitudinal Regions of the Korean Peninsula

Original Article

The Korean Journal of Parasitology 2011; 49(4): 385-398.

Published online: December 16, 2011

DOI: https://doi.org/10.3347/kjp.2011.49.4.385

Prevalence of Clonorchis sinensis Metacercariae in Freshwater Fish from Three Latitudinal Regions of the Korean Peninsula

Shin-Hyeong Cho¹, Woon-Mok Sohn², Byoung-Kuk Na², Tong-Soo Kim³, Yoon Kong⁴, Keeseon Eom⁵, Won-Seok Seok⁶, Taejoon Lee⁶

¹Division of Malaria and Parasitic Diseases, National Institute of Health, Centers for Disease Control and Prevention, Osong 363-951, Korea.

²Department of Parasitology and Institute of Health Sciences, Gyeongsang National University School of Medicine, Jinju 660-751, Korea.

³Department of Parasitology and Inha Research Institute for Medical Sciences, Inha University College of Medicine, Incheon 400-712, Korea.

⁴Department of Molecular Parasitology, Sungkyunkwan University School of Medicine, Center for Molecular medicine, Samsung Biomedical Research Institute, Suwon 440-746, Korea.

⁵Department of Parasitology and Medical Research Institute, Chungbuk National University College of Medicine, Cheongju 360-763, Korea.

⁶Infection Disease Intelligence Division, Gangwon Institute of Health and Environment, Chuncheon 200-822, Korea.

Corresponding author (wmsohn@gnu.ac.kr)

Received September 20, 2011 Revised October 31, 2011 Accepted November 03, 2011

(open-access, http://creativecommons.org/licenses/by-nc/3.0):

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

A large-scale survey was conducted to investigate the infection status of fresh water fishes with Clonorchis sinensis metacercariae (CsMc) in 3 wide regions, which were tentatively divided by latitudinal levels of the Korean peninsula. A total of 4,071 freshwater fishes were collected from 3 regions, i.e., northern (Gangwon-do: 1,543 fish), middle (Chungcheongbuk-do and Gyeongsangbuk-do: 1,167 fish), and southern areas (Jeollanam-do, Ulsan-si, and Gyeongsangnam-do: 1,361 fish). Each fish was examined by the artificial digestion method from 2003 to 2010. In northern areas, only 11 (0.7%) fish of 2 species, Pungtungia herzi and Squalidus japonicus coreanus from Hantan-gang, Cheolwon-gun, Gangwon-do were infected with av. 2.6 CsMc. In middle areas, 149 (12.8%) fish were infected with av. 164 CsMc. In southern areas, 538 (39.5%) fish were infected with av. 159 CsMc. In the analysis of endemicity in 3 regions with an index fish, P. herzi, 9 (6.2%) of 146 P. herzi from northern areas were infected with av. 2.8 CsMc. In middle areas, 34 (31.8%) of 107 P. herzi were infected with av. 215 CsMc, and in southern areas, 158 (92.9%) of 170 P. herzi were infected with av. 409 CsMc. From these results, it has been confirmed that the infection status of fish with CsMc is obviously different among the 3 latitudinal regions of the Korean peninsula with higher prevalence and burden in southern regions.

Key words: Clonorchis sinensis, metacercaria, freshwater fish, prevalence, latitudinal level

INTRODUCTION

Recent trends of helminthic infections in the Republic of Korea are characterized by a remarkable decrease of soil-transmitted nematodiases and moderate endemicity of foodborne trematode (FBT) infections. Among FBT infections prevailing in the Republic of Korea, clonorchiasis has been known as the most important endemic disease, and its endemicity has maintained at relatively high levels in riverside areas [1-6]. Especially, in 1981, Seo et al. [1] reported prevalence rates of clonorchiasis among the residents in 7 major rivers, Nakdong-gang (River) (40.2%), Youngsan-gang (30.8%), Seomjin-gang (17.3%), Tamjin-gang (15.9%), Han-gang (15.7%), Gum-gang (12.0%), and Mangyeong-gang (8.0%). In 2008, Cho et al. [5] reported the egg positive rates of residents living in 4 river basins, Nakdong-gang (17.1%), Seomjin-gang (11.2%), Youngsan-gang (5.5%), and Gum-gang (4.6%), located in southern parts of Korea. Although the Korea Association of Health Promotion (KAHP) and the Korea Center for Disease Control and Prevention (KCDCP) have been performing control programmes of clonorchiasis for more than 20 years, clonorchiasis is still prevalent throughout the country [3,6].

Clonorchiasis is contracted by eating raw or undercooked fish intermediate hosts containing the metacercariae of C. sinensis. As the second intermediate hosts of C. sinensis, total 40 species of freshwater fishes have been reported in Korea [2,7]. Among them, some species, such as Pseudorasbora parva, Pungtungia herzi, Sarcocheilichthys spp., Squalidus spp., and Pseudogobio esocinus, have been known as the more susceptible hosts to cercariae, and they have sometimes enormous amount of metacercariae [8-12].

On the other hand, the survey on the infection status of FBT metacercariae in intermediate hosts is one of the important epidemiological indices together with surveys on adult worm infections in the definitive and reservoir hosts. Many Korean workers have investigated the infection status of C. sinensis metacercariae (CsMc) in fishes from various endemic areas to estimate the endemicity of clonorchiasis [8,9,11-17]. Especially, Kim et al. [12] investigated 677 freshwater fish of 21 species to know the current infection status with CsMc in Korea. However, large-scale surveys have not been conducted to compare the prevalence and density of CsMc in freshwater fishes collected by different latitudinal levels of the Korean peninsula. Therefore, in the present study, we investigated on the infection status of CsMc in freshwater fish from 3 wide regions, which were tentatively divided by the latitudinal levels of the Korean peninsula.

MATERIALS AND METHODS

Surveyed areas

Surveyed areas were largely divided into 3 latitudinal regions of the Korean peninsula (Fig. 1). The northern area was comprised of 7 administrative regions of Gangwon-do, ① Inje-gun, ② Hongcheon-gun, ③ Cheolwon-gun, ④ Yanggu-gun, ⑤ Yangyang-gun, ⑥ Youngweol-gun, and ⑦ Samcheok-si, which are located over 37° North Latitude. The middle area contained 10 regions of Chungcheongbuk-do (⑧ Gum-gang in Okcheon-gun, ⑨ Cheong-cheon in Goisan-gun, and ⑩ Daecheong-ho), and Gyeongsangbuk-do (⑪ Ahndong-si, ⑫ Sangju-si, ⑬ Bonghwa-gun, ⑭ Yecheon-gun, ⑮ Youngyang-gun, ⑯ Youngdeok-gun, and ⑰ Gunwi-gun), which are located between 36° and 37° North Latitude. The southern area was comprised of 8 administrative regions of Jeollanam-do (⑱ Gokseong-gun, ⑲ Gurye-gun, ⑳ Naju-si, ㉑ Gangjin-gun, ㉒ Jangheung-gun, and ㉓ Boseong-gun), Ulsan Metropolitan City (㉔ Taehwa-gang) and Gyeongsangnam-do (㉕ Sancheong-gun), which are located below 36° North Latitude.

Freshwater fishes examined

In western parts of Gangwon-do, we collected 678 freshwater fishes (36 species) from 4 localities, Soyang-gang (Inje-gun in October 2003 and April 2004), Hongcheon-gang (Hongcheon-gun in October 2003, and July and October 2010), Hantan-gang (Cheolwon-gun in April 2005 and October 2010), and Hwa-gang (Cheolwon-gun in June 2010) in Gangwon-do. We also collected 865 fishes (32 species) from 5 localities of eastern parts of Gangwon-do, Sooip-cheon (Yanggu-gun), Namdae-cheon (Yangyang-gun), Dong-gang (Youngweol-gun), Osip-cheon, and Gagok-cheon (Samcheok-si) 2 times in June and October 2009. The numbers and species of fish examined are shown in Tables 1 and 2.

In middle regions, a total of 451 fishes (32 species) were collected from 3 sites, Gum-gang (Okcheon-gun in April and September 2006), Cheong-cheon (stream in Goisan-gun on June 2003) and Daecheong-ho (Lake, on June 2003), located in Chungcheongbuk-do. The numbers and species of fish examined are shown in Table 3. To investigate the infection status of CsMc in fishes from the upper reaches of Nakdong-gang, we collected total 716 freshwater fishes (35 species) from 7 localities, Ahndong-si, Sangju-si, Bonghwa-gun, Yecheon-gun, Youngyang-gun, Youngdeok-gun and Gunwi-gun, Gyeongsangbuk-do in October and November, 2008 (Table 4).

In western parts of southern localities, 452 freshwater fishes (35 species) were collected from 6 localities, Seomjin-gang (Gokseong-gun in September 2004 and May 2005) (Gurye-gun in September 2004), Youngsan-gang (Naju-si in October 2005), Tamjin-gang (Gangjin-gun and Jangheung-gun, in October 2005) and Boseong-gang (Boseong-gun in October 2005), in Jeollanam-do. The numbers and species of fish examined are shown in Table 5. In eastern parts, we also collected 909 freshwater fishes (24 species) from Taehwa-gang (Ulsan Metropolitan City in April and September 2006) and Yangcheon-gang (Sancheong-gun in each October of 2006 and 2007, June and July 2010) in Gyeongsangnam-do (Table 6).

Examination methods

All collected fishes with ice were transferred to the laboratory of the Department of Parasitology, Gyeongsang National University School of Medicine, Jinju, Korea. After identification of fish species [18], they were individually ground with a mortar with a pestle or a grinder. Each ground fish meat was mixed with artificial gastric juice and the mixture was incubated at 36℃ for 2-3 hr. The digested material was filtered with 1×1 mm of mesh, and washed with 0.85% saline untill the supernatant is clear. The sediment was carefully examined under a stereomicroscope. The metacercariae of C. sinensis were collected based on their general features [7], and they were counted to get hold of the infection densities by fish species.

RESULTS

Infection status of freshwater fish from northern areas

The metacercariae of C. sinensis were found in only 2 fish species, P. herzi and Squalidus japonicus coreanus, collected from Hantan-gang in Cheolwon-gun, Gangwon-do. Total 6 CsMc were detected in 3 out of 8 P. herzi examined in April, 2005. They were also detected in 6 (85.7%) of 7 P. herzi and both 2 of S. japonicus coreanus examined in October 2010. The metacercarial densities were 3.2 and 2.0 per infected fish. However, they were not found in fishes from 7 localities, Hongcheon-gang in Hongcheon-gun, Hwa-gang in Cheolwon-gun, Sooip-cheon in Yanggu-gun, Namdae-cheon in Yangyang-gun, Dong-gang in Youngweol-gun, and Osip-cheon and Gagok-cheon in Samcheok-si, Gangwon-do.

Infection status of freshwater fish from middle areas

A total of 50 CsMc were detected in 22 (10 species) of 356 freshwater fish (28 species) collected from Gum-gang, and total 27 metacercariae were found in 6 (3 species) of 53 fish from Cheong-cheon. Their infection status by fish species were as shown in Table 7. No CsMc were found in 42 fishes from Daecheong-ho.

CsMc were found in 3 (12.5%) of 24 P. herzi and only 1 (4.8%) Zacco platypus from Ahndong-si, and their average densities were 62 in P. herzi and only 1 in Z. platypus infected. They were also detected in all 6 P. herzi and only 1 of 2 Acanthorhodeus gracilis from Sangju-si, and their average densities were 11 in P. herzi and only 1 in A. gracilis infected. Total 46 CsMc were detected in 10 (35.7%) of 28 Squalidus gracilis majimae from Youngdeok-gun. However, CsMc were not found in other fishes from Bonghwa-gun.

A total of 68 CsMc were found in 9 (15.8%) out of 57 fish of 7 species, Ladislabia taczanowskii, Culter brevicauda, P. herzi, Z. platypus, Pseudogobio esocinus, Hemibarbus longirostris. and Hemibarbus labeo from Yecheon-gun. Total 31 (36.0%) fishes of 6 species, P. herzi, Squalidus chankaensis tsuchigae, Microphysogobio koeensis, Coreoleuciscus splendidus, Acheilognathus signifer and Z. platypus, out of 86 fish in 12 species from Youngyang-gun, were infected with 1-630 CsMc (av. 126 per fish). Among 136 fishes of 16 species collected from Gunwi-gun, 70 (51.5%) of 14 species were infected with 1-2,105 CsMc (av. 287). The infection status in fishes from Yecheon-gun, Youngyang-gun, and Gunwi-gun were detailed in Table 8.

Infection status of freshwater fish from southern areas

Among 191 fishes (22 species) from Seomjin-gang in Gokseong-gun, 42 (13 species) were infected with 2,496 CsMc (av. 59), and 37 fishes (9 species) from Seomjin-gang in Guryu-gun were infected with total 1,390 CsMc (av. 49). Their infection status by fish species were shown in Table 9.

A total of 1,831 CsMc (av. 80) were detected in 23 (9 species) of 65 freshwater fish (11 species) from Youngsan-gang in Naju-si. Among 58 fishes (11 species) from Tamjin-gang in Gangjin-gun, 39 (9 species) were infected with total 8,020 CsMc (av. 206), and a total of 162 CsMc (av. 32) were detected in 5 (4 species) of 18 freshwater fish (10 species) collected from Boseong-gang in Boseong-gun, Jeollanam-do. Infection status by fish species from 3 aforementioned regions were presented in Table 10. No CsMc were found in 52 fish from Tamjin-gang in Janghung-gun, Jeollanam-do.

Total 175 CsMc (av. 22) were detected in 8 (32.0%) of 25 S. chankaensis tsuchigae, and 5 CsMc in 3 (5.0%) Z. platypus collected from Taehwa-gang in Ulsan Metropolitan City. Total 381 (48.2%) of 790 fish from Yangcheon-gang in Sancheong-gun, Gyeongsangnam-do were infected with 1-2,345 CsMc (av. 187). The infection status by fish species and examination year were shown in Table 11.

Comparative prevalence and density of CsMc in freshwater fish from 3 regions

Among 1,543 fish from northern areas, only 11 (0.7%) of 2 species, P. herzi and S. japonicus coreanus, from Hantan-gang in Cheolwon-gun, were infected with total 29 CsMc (av. 2.6 per infected fish). Total 149 (12.8%) of 1,167 fish from middle areas were infected with total 24,384 CsMc (av. 163.7). Of 1,361 fish from southern areas, 538 (39.5%) were infected with total 85,428 CsMc (av. 158.8).

In an analysis with an index fish, P. herzi, total 25 CsMc (av. 2.8) were detected in 9 (6.2%) of 146 fishes from northern areas. Among 107 P. herzi from middle areas, 34 (31.8%) were infected with total 7,300 CsMc (av. 214.7). Total 158 (92.9%) of 170 P. herzi collected from southern areas were infected with total 64,674 CsMc (av. 409.3). On the other hand, no CsMc were found in 247 Z. platypus from northern areas. Of 223 Z. platypus from middle areas, 17 (7.6%) were infected with total 147 CsMc (av. 8.6). Total 13 (5.7%) of 228 Z. platypus from southern areas were infected with 139 CsMc (av. 10.7) (Table 12).

DISCUSSION

As the second intermediate hosts of C. sinensis, total 102 species of freshwater fishes (59 genera, 15 families) have been reported in China, including Taiwan, and total 40 species (31 genera, 6 families) have been listed in the Republic of Korea [7,19]. In the present study, CsMc were detected in 36 fish species. Of the 36 positive fish species, 28 have been already known as the second intermediate hosts of C. sinensis. However, 8 species, namely, Pseudopuntungia nigra, Rhynchocypris oxycephalus, Ladislabia taczanowskii, Microphysogobio longidorsalis, Acheilognathus majusculus, Acheilognathus koreensis, Acanthorhodeus macropterus, and Odontobutis platycephala, have not been listed in the Republic of Korea [7]. Among aforementioned 8 new fish hosts, R. oxycephalus is the same fish species with Phoxinus (or Morocco) oxycephalus, which has been already recorded. Accordingly, total 47 fish species (34 genera, 7 families) are included among the second intermediate hosts of C. sinensis in the Republic of Korea.

The successful sampling of subjected materials is one of the important factors in epidemiological surveys. A satisfactory fish collection is not easy in surveys like the present study. Fish ecologies are variable by natural conditions, and collected fish species are different by the catching methods (netting, casting net, and trapping) and timings. Although a total of 4,071 freshwater fish were examined in the present study, the fish examined more than 200 in number were only 7 species, i.e. Z. platypus (698), P. herzi (423), Zacco temminckii (344), Pseudogobio esocinus (236), C. auratus (204), Coreoperca herzi (203), and C. splendidus (200). Among 7 major fish species examined, Z. platypus and P. herzi were predominant, and they were evenly collected in each of 3 regions. Total 247, 223, and 228 Z. platypus and 146, 107, and 170 P. herzi were examined in each of 3 regions, northern, middle, and southern areas of Korea. Therefore, these 2 fish species are good to use as index fish species to compare the endemicities of C. sinensis infection in 3 regions of the present study. Until now the susceptible fish host for CsMc, P. parva, has been used as an index species for distribution of C. sinensis at certain areas [10,12,20-22]. However, in this study, their number examined were limited.

By the present study, it is confirmed again that the southern areas are highly endemic for clonorchiasis in Korean peninsula [1-6]. The positive rates and infection densities of CsMc are higher in over all fish examined, as well as in P. herzi, from these southern areas, although they are exceptionally higher in fish species, i.e. P. herzi, P. esocinus, S. gracilis majimae and S. japonicus coreanus, from Gunwi-gun, Gyeongsangbuk-do. In the analysis with the index fish, P. herzi, the positive rates are relatively proportioned with the average metacercarial density per infected fish. Therefore, the highly susceptible fish species, P. herzi, can be the real index fish of clonorchiasis transmission in the natural condition, and the presence of metacercariae in this fish species may suggest the maintaining of C. sinensis life cycle in subjected areas.

On the other hand, in case of Z. platypus, CsMc were not detected in 247 fish from northern areas. Total 17 (7.6%) out of 223 Z. platypus from middle areas were infected with 147 CsMc, and 13 (5.7%) out of 228 fishes from southern areas were infected with 139 CsMc. From the above findings, we could not find any special trend in the endemicity of C. sinensis infection in 3 regions. Therefore, it is confirmed that a less susceptible fish species, like Z. platypus, is unsuitable as an index fish, although they are widely collected in 3 regions as dominant fish species.

CsMc were not found in all fishes from 9 localities in northern areas except 2 species, P. herzi and S. japonicus coreanus, from Hantan-gang in Cheolwon-gun, Gangwon-do. In the study by Kim et al. [12], all the fish from upper regions of Cheongju, Chungcheongbuk-do were negative for CsMc, even though the number of susceptible fishes examined were limited. It is interesting that CsMc were detected only in fishes from Hantan-gang in northern areas. First of all, as an important epidemiologic factor for clonorchiasis, the availability of the snail intermediate host, Parafossarulus manchouricus, should be investigated in the near future in Hantan-gang in Cheolwon-gun, Gangwon-do. There have been few studies on the CsMc infection status of fishes from Gangwon-do, whreas many studies have been performed to investigate the infection status of intestinal flukes, including Metagonimus spp. in fishes from Gangwon-do [23-28]. It is probably due to the reasion that Gangwon-do is endemic for intestinal fluke infections rather than clonorchiasis.

Among the 47 fish species listed as the second intermediate hosts of C. sinensis in Korea, Hypomesus olidus (the pond smelt) and Z. platypus are favoritely eaten raw in Korea. Fortunately, they are relatively unsusceptible for CsMc. In our study, CsMc were not found in 247 Z. platypus from Gangwon-do, and in extensive examinations of pond smelts from several lakes in Korea previously by Cho et al. [29]. Moreover, in the present study, they were not detected in 1,532 fishes from Gangwon-do, and in 42 fish from Daecheong-ho. However, Park et al. [30] detected CsMc in H. olidus and Z. platypus from Soyang-ho and Daecheong-ho. Especially, it was remarkable that total 369 CsMc were detected in 100 H. olidus from Daecheong-ho [30]. Judging by aforementioned data and ecological and biological characteristics of C. sinensis, the findings of Park et al. (2004) need further verification.

The positive rates and densities of CsMc were relatively high in fishes from the upper reaches of Nakdong-gang in Youngyang-gun and Gunwi-gun, Gyeongsangbuk-do. Of the 86 fishes from Youngyang-gun, 31 (36.0%) were infected with av. 126 CsMc, and 70 (51.5%) of 136 fishes from Gunwi-gun were infected with av. 287 CsMc. Chung et al. [31] examined 794 fishes, including 140 P. herzi from Youngyang-gun, and they detected 2.1 CsMc per gram of muscles from only 10 (23.3%) of 43 Gnathopogon atromaculatus (=Squalidus chankaensis tsuchigae) examined. Kim et al. [32] detected 11.6 CsMc per gram of muscles in 61 (43.9%) of 139 fishes from Wicheon in Uiseong-gun, Gyeongsangbuk-do. Accordingly, we could determine that the endemicity of CsMc in fishes from Youngyang-gun and Gunwi-gun are a little higher in the present study than in previous reports.

There have been few studies that examined the infection status of CsMc in fishes from Jeollanam-do. Kim et al. [12] roughly revealed the distribution of fishes infected with CsMc based on individual fish species. The present study showed a more detailed information on the endemicity of CsMc in fishes from 6 localities, Gokseong-gun, Gurye-gun, Naju-si, Gangjin-gun, Jangheung-gun, and Boseong-gun, in Jeollanam-do. The endemicity was relatively higher in fishes from 5 localities except Jangheung-gun. Especially, it is interesting to note that the endemicity of C. sinensis in fishes from Gangjin-gun is high, because Gangjin-gun has been well known as a highly endemic area of metagonimiasis [33,34].

Studies on the CsMc infection status of fishes from Taehwa-gang in Ulsan Metropolical City were performed by some workers. Joo [15,35] examined 504 and 697 freshwater fishes from Taehwa-gang, and reported 31 (6.2%) and 126 (18.1%) fish infected with CsMc. Rim et al. [36] also reported 29 (47.5%) CsMc positive fishes, of 2 species, P. parva and S. chankaensis tsuchigae, out of 61 fishes examined in Taehwa-gang. In the present study, we detected total 180 CsMc in 11 (9.2%) fishes of only 2 species, S. chankaensis tsuchigae, and Z. platypus, out of 119 fishes from Taehwa-gang. Therefore, we could determine that the endemicity of CsMc in the present study is much lower than those in the previous studies.

Bae et al. [37] extensively surveyed on C. sinensis infections in the first and second intermediate hosts, definitive hosts, and inhabitants, residing along Nam-gang, in Gyeongsangnam-do. Especially on the second intermediate hosts, they reported that 83 (34.7%) of 239 fishes, including 64 P. parva, were infected with CsMc. In the present study, we examined total 790 freshwater fishes from Yangcheon-gang, a stream of Nam-gang, in Sancheong-gun, Gyeongsangnam-do, and detected av. 187 CsMc from 381 (48.2%) fishes. Until now the endemicity of CsMc in fishes from streams of Nam-gang, including Yangcheon-gang, is as high as in old days. It seems to be one of the reasons why Sancheong-gun is the most highly endemic area of clonorchiasis around the whole country [5]. Therefore, inhabitants residing in endemic areas, like Sancheong-gun, should pay attention to clonorchiasis, and consumption of raw freshwater fish naturally produced in these areas should be avoided.

ACKNOWLEDGMENTS

This study was supported by an anti-communicable diseases control program (NIH 348-6111-215) and a project on the parasite fauna of the Republic of Korea and management of parasitic diseases cyber-musium (2008-E00165-00) of National Institute of Health, Ministry of Health and Welfare, the Republic of Korea. We thank Young-Kil Kim (Division of Public Health Policy, Province of Gyeongsangbuk-do) and Sook-Nam Hwang (Division of Microbiology, Ulsan Institute of Health and Environment), for their help in collection of freshwater fish, and A-Ra Cho, Hae-In Ryu, Jung-A Kim, and Hee-Joo Kim (Department of Parasitology, Gyeongsang National University School of Medicine, Jinju, Korea), for their help in examination of fishes.

REFERENCES

1. 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;19:137-150.

2. Rim HJ. The current pathobiology and chemotherapy of clonorchiasis. Korean J Parasitol 1986;24(suppl):1-141.

3. Korean Association of Health Promotion (KAHP). Prevalence of intestinal parasitic infection in Korea-the 7th Report. 2004, Seoul, Korea. KAHP. pp 1-275.

4. Hong ST, Hong SJ. Clonorchis sinensis and clonorchiasis in Korea. Food-Borne Helminthiasis in Asia. Asian Parasitology 2005;1:35-56.

5. Cho SH, Lee KY, Lee BC, Cho PY, Cheun HI, Hong ST, Sohn WM, Kim TS. Prevalence of clonorchiasis in southern endemic areas of Korea in 2006. Korean J Parasitol 2008;46:133-137. PMID: 18830051.

6. Kim TS, Cho SH, Huh S, Kong Y, Sohn WM, Hwang SS, Chai JY, Lee SH, Park YK, Oh DK, Lee JK. A nationwide survey on the prevalence of intestinal parasitic infections in the Republic of Korea, 2004. Korean J Parasitol 2009;47:37-47. PMID: 19290090.

7. Sohn WM. Fish-borne zoonotic trematode metacercariae in the Republic of Korea. Korean J Parasitol 2009;47(suppl):S103-S113. PMID: 19885326.

8. Rhee JK, Lee HI, Baek BK, Kim PG. Survey on encysted cercariae of trematodes from freshwater fishes in Mangyeong riverside area. Korean J Parasitol 1983;21:187-192.

9. Rhee JK, Rim MH, Baek BK, Lee HI. Survey on encysted cercariae of trematodes from freshwater fishes in Tongjin riverside areas in Korea. Korean J Parasitol 1984;22:190-202.

10. Kang SY, Kim SI, Cho SY. Seasonal variations of metacercarial density of Clonorchis sinensis in fish intermediate host, Pseudorasbora parva. Korean J Parasitol 1985;23:87-94.

11. Sohn WM, Choi YS. Infection status with trematode metacercariae in the fresh-water fish from Chunamchosuchi (pond), Uichang-gun, Kyongsangnam-do, Korea. Korean J Parasitol 1997;35:165-170. PMID: 9335181.

12. Kim EM, Kim JL, Choi SY, Kim JW, Kim S, Choi MH, Bae YM, Lee SH, Hong ST. Infection status of freshwater fish with metacercariae of Clonorchis sinensis in Korea. Korean J Parasitol 2008;46:247-251. PMID: 19127331.

13. Choi DW. Clonorchis sinensis in Kyungpook Province, Korea 2. Demonstration of metacercaria of Clonorchis sinensis from fresh water fish. Korean J Parasitol 1976;14:10-16.

14. Hwang JT, Choi DW. Changing pattern of infestation with larval trematodes from freshwater fish in river Kumho, Kyungpook Province, Korea. Kyungpook Univ Med J 1980;21:460-475.

15. Joo CY. Changing pattern of infection with digenetic larval trematodes from freshwater fish in river Taewha, Kyongnam Province. Korean J Parasitol 1988;26:263-274.

16. Kong HH, Choi BR, Moon CH, Choi DW. Larval digenetic trematodes from freshwater fish in river Miryang, Korea. Jpn J Parasitol 1995;44:112-1184.

17. Joo CY, Chung MS, Kim SJ, Kang CM. Changing patterns of Clonorchis sinensis infections in Kyongbuk, Korea. Korean J Parasitol 1997;35:155-164. PMID: 9335180.

18. Kim IS, Park JY. Freshwater fishes of Korea. 2002, Seoul, Korea. KyoHak Publishing Co. pp 1-465.

19. Xu LQ, Yu SH, Chen YD. In Arizono N, Chai JY, Nawa Y, Takahashi Y eds, Clonorchiasis sinensis in China. Asian Parasitology, Vol. 1. Food-Borne Helminthiasis in Asia. 2004, Chiba, Japan. Federation of Asian Parasitologists. pp 1-26.

20. Kim YK, Kang SY, Lee SH. Study on the frequency distribution of the metacercarial density of Clonorchis sinensis in fish host, Pseudorasbora parva. Korean J Parasitol 1979;17:127-131 (in Korean).

21. Kim KH, Yie JH, Joo KH, Lee JS, Rim HJ. Studies on the infection rate and distribution pattern of metacercaria of Clonorchis sinensis in Pseudorasbora parva. Korean J Rural Med 1989;14:44-53 (in Korean).

22. Park JK, Chung DI, Choi DW. Relationship between infestation with Clonorchis sinensis metacercariae and length of freshwater fish. Kyungpook Univ Med J 1991;32:297-304 (in Korean).

23. Ahn YK. Epidemiological studies on Metagonimus yokogawai infection in Samcheok-gun, Kangwon-do, Korea. Korean J Parasitol 1984;22:161-170 (in Korean).

24. Ahn YK, Ryang YS. Experimental and epidemiological studies on the life cycle of Echinostoma hortense Asada, 1926 (Trematoda: Echinostomatidae). Korean J Parasitol 1986;24:121-136 (in Korean).

25. Ahn YK, Chung PR, Lee KT, Soh CT. Epidemiological survey on Metagonimus yokogawai infection in the Eastern coast of Kangwon Province, Korea. Korean J Parasitol 1987;25:59-68 (in Korean).

26. Ahn YK, Ryang YS. Epidemiological studies on Metagonimus infection along the Hongcheon river, Kangwon Province. Korean J Parasitol 1988;26:207-213 (in Korean).

27. Sohn WM, Hong ST, Chai JY, Lee SH. Infection status of sweetfish from Kwangjung-stream and Namdae-stream in Yangyang-gun, Kangwon-do with the metacercariae of Metagonimus yokogawai. Korean J Parasitol 1990;28:253-255 (in Korean).

28. Chai JY, Huh S, Yu JR, Kook J, Jung KC, Park EC, Sohn WM, Hong ST, Lee SH. An epidemiological study of metagonimiasis along the upper reaches of the Namhan river. Korean J Parasitol 1993;31:99-108. PMID: 8343462.

29. Cho SH, Sohn WM, Song HJ, Choi TG, Oh CM, Kong Y, Kim TS. Infection status of pond smelts, Hypomesus olidus and other freshwater fishes with trematode metacercariae in 6 large lakes. Korean J Parasitol 2006;44:243-246. PMID: 16969063.

30. Park JH, Guk SM, Kim TY, Shin EH, Lin A, Park JY, Kim JL, Hong ST, Chai JY. Clonorchis sinensis metacercarial infection in the pond smelt Hypomesus olidus and minnow Zacco platypus collected from the Soyang and Daechung Lakes. Korean J Parasitol 2004;42:41-44. PMID: 15060339.

31. Chung DI, Kim YI, Lee KR, Choi DW. Epidemiological studies of digenetic trematodes in Yongyang County, Kyungpook Province. Korean J Parasitol 1991;29:325-338.

32. Kim HK, Moon CH, Kong HH, Choi DW. Infestation of Clonorchis sinensis metacercaria from freshwater fish in river Wichon. Kyungpook Univ Med J 1993;34:17-23.

33. 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;20:28-32 (in Korean).

34. Lee JJ, Kim HJ, Kim MJ, Lee JWY, Jung BK, Lee JY, Shin EH, Kim JL, Chai JY. Decrease of Metagonimus yokogawai endemicity along the Tamjin river basin. Korean J Parasitol 2008;46:289-291. PMID: 19127339.

35. Joo CY. Epidemiological studies of Clonorchis sinensis in vicinity of River Taewha, Kyungnam Province, Korea. Korean J Parasitol 1980;18:199-214.

36. Rim HJ, Kim KH, Joo KH, Kim SJ, Eom KS, Chung MS. The infestation status and changing patterns of human infecting metacercariae in freshwater fish in in Kyongsang-do and Kyonggi-do, Korea. Korean J Parasitol 1996;34:95-105. PMID: 8925250.

37. Bae KH, Ahn YK, Soh CT, Tsutsumi H. Epidemiological studies on Clonorchis sinensis infection along the Nam-river in Gyeongnam Province, Korea. Korean J Parasitol 1983;21:167-186 (in Korean).

Fig. 1

The surveyed areas. The northern area located over 37° North Latitude is comprised of 7 administrative regions of Gangwon-do (① Inje-gun: Soyang-gang, ② Hongcheon-gun: Hongcheon-gang, ③ Cheolwon-gun: Hantan-gang and Hwa-gang, ④ Yanggu-gun: Sooip-cheon, ⑤ Yangyang-gun: Namdae-cheon, ⑥ Youngweol-gun: Dong-gang and ⑦ Samcheok-si: Osip-cheon and Gagok-cheon). The middle area located between 36° and 37° North Latitude is contained 3 regions of Chungcheongbuk-do (⑧ Okcheon-gun: Gum-gang, ⑨ Goisan-gun: Cheong-cheon and ⑩ Daecheong-ho), and 7 regions of Nakdong-gang (⑪ Ahndong-si, ⑫ Sangju-si, ⑬ Bonghwa-gun, ⑭ Yecheon-gun, ⑮ Youngyang-gun, ⑯ Youngdeok-gun and ⑰ Gunwi-gun) in Gyeongsangbuk-do. The southern area located below 36° North Latitude is comprised of 6 administrative regions of Jeollanam-do (⑱ Gokseong-gun: Seomjin-gang, ⑲ Gurye-gun: Seomjin-gang, ⑳ Naju-si: Youngsan-gang, ㉑ Gangjin-gun: Tamjin-gang, ㉒ Jangheung-gun: Tamjin-gang and ㉓ Boseong-gun: Boseong-gang), and ㉔ Ulsan Metropolitan City (Taehwa-gang) and ㉕ Sancheong-gun (Yangcheon-gang) in Gyeongsangnam-do.

Table 1.

Fishes^a collected from northern regions (Gangwon-do), Korea

Species of fish	No. of fish collected from 6 localites^b
Species of fish	①	②-1	②-2	③-1	③-2	③-3	Total
Cypriniforms
Zacco platypus	40	10	20	16	30	3	119
Pungtungia herzi	14	20	25	8	7	13	87
Zacco temminckii	6	-	16	19	30	10	81
Hemibarbus longirostris	5	-	20	14	3	12	54
Pseudogobio esocinus	10	1	23	5	8	3	50
Coreoleuciscus splendidus	5	3	18	19	-	2	47
Microphysogobio longidorsalis	-	-	20	4	-	8	32
Carassius auratus	6	-	2	2	3	5	18
Acheilognathus signifer	-	10	-	-	-	4	14
Hemibarbus labeo	10	-	1	2	-	-	13
Acheilognathus majusculus	-	-	6	-	6	-	12
Cyprinus capio	5	-	-	-	-	-	5
Acheilognathus yamatsutae	-	-	-	5	-	-	5
Acheilognathus rhombeus					5	-	5
Opsariichthys uncirostris	3	-	2	-	-	-	5
Pseudopungtungia tenuicorpa	1	3	-	-	-	-	4
Pseudobagrus fulvidraco	-	-	-	4	-	-	4
Hemibarbus mylodon	-	-	-	1	3	-	4
Acanthorhodeus gracills	-	-	-	3	-	-	3
Acheilognathus lanceolatus	-	-	-	-	1	2	3
Hemiculter leucisculus	3	-	-	-	-	-	3
Koreocobitis rotundicaudata	-	-	-	3	-	-	3
Orthrias toni	-	3	-	-	-	-	3
Rhynchocypris steidachneri	-	-	-	-	3	-	3
Rhynchocypris oxycephalus	-	-	-	2	-	-	2
Squalidus japonicus coreanus	-	-	-	-	2	-	2
Sarcocheilichthys nigripinnis	-	-	-	-	1	-	1
Microphysogobio jeoi	-	-	-	-	1	-	1
Abbottina springeri	1	-	-	-	-	-	1
Abbotina revulais	-	1	-	-	-	-	1
Siluriformes
Liobagrus andersoni	4	10	-	-	-	-	14
Leiocassis ussuriensis	3	-	-	-	-	-	3
Perciformes
Coreoperca herzi	-	15	20	3	5	7	50
Siniperca scherzeri	7	-	11	-	-	-	18
Odontobutis platycephala	-	6	2	-	-	-	8
Total	123	82	186	110	108	69	678

^a Total 678 freshwater fishes of 36 species were examined.

^b ① Inje-gun (Soyang-gang); ②-1 Hongcheon-gun (Hongcheon-gang, 2003); ②-2 Hongcheon-gun (Hongcheon-gang, 2010); ③-1 Cheolwon-gun (Hantan-gang, 2005); ③-2 Cheolwon-gun (Hantan-gang, 2010); ③-3 Cheolwon-gun (Hwa-gang, 2010).

Table 2.

Fishes^a collected from northern regions (Gangwon-do), Korea (2009)

Species of fish	No. of fish collected from 5 localities^b
Species of fish	④	⑤	⑥	⑦-1	⑦-2	Total
Cypriniforms
Zacco platypus	26	30	30	23	19	128
Zacco temminckii	23	30	30	-	20	103
Coreoleuciscus splendidus	27	-	30	30	8	95
Pungtungia herzi	11	15	16	-	17	59
Tribolodon hakonensis	-	30	-	21	-	51
Microphysogobio longidorsalis	25	-	25	-	-	50
Rhynchocypris oxycephalus	10	3	-	1	25	39
Hemibarbus longirostris	14	-	16	-	-	30
Pseudogobio esocinus	11	-	10	-	-	21
Gobiobotia brevibarba	-	-	18	-	-	18
Carassius auratus	14	2	-	-	-	16
Hemibarbus labeo	-	-	13	-	-	13
Koreocobitis rotundicaudata	-	-	13	-	-	13
Hemibarbus mylodon	2	-	10	-	-	12
Acanthorhodeus macropterus	-	-	10	-	-	10
Orthrias toni	-	-	-	8	-	8
Opsariichthys uncirostris	5	-	-	-	-	5
Misgurnus mizolepis	-	-	5	-	-	5
Ladislabia taczanowskii	-	-	-	3	-	3
Gobiobotia macrocephala	-	-	3	-	-	3
iksookimia koreensis	-	-	2	-	-	2
Cyprinus capio	1	-	-	-	-	1
Pseudobagrus fulvidraco	-	-	1	-	-	1
Osmeriformes
Plecoglossus altivelis	-	25	-	29	-	54
Salmoniformes
Onchorhynchus masou masou	-	5	-	2	3	10
Siluriformes
Liobagrus andersoni	10	-	3	-	-	13
Silurus asotus	-	-	1	-	-	1
Perciformes
Coreoperca herzi	17	10	15	-	-	42
Chaenogobius urotaenia	-	-	-	19	8	27
Tridentiger brevispinis	-	-	-	15	9	24
Rhinogobius giurinus	-	-	-	4	-	4
Acanthogobius pflaumi	-	4	-	-	-	4
Total	196	154	251	155	109	865

^a Total 865 freshwater fishes of 32 species were examined.

^b 5 localities, ④ Yanggu-gun (Sooip-cheon); ⑤ Yangyang-gun (Namdae-cheon); ⑥ Youngweol-gun (Dong-gang); ⑦-1 Samcheok-si (Osip-cheon); ⑦-2 Samcheok-si (Gagok-cheon).

Table 3.

Fishes^a collected from middle regions (Chungcheongbuk-do), Korea

Species of fish	No. of fish collected from 3 localities^b
Species of fish	⑧	⑨	⑩	Total
Cypriniforms
Zacco platypus	43	20	2	65
Acheilognathus lanceolatus	49	-	2	51
Acanthorhodeus gracilis	41	-	-	41
Hemibarbus labeo	34	-	5	39
Hemiculter eigenmanni	28	-	4	32
Pungtungia herzi	25	6	-	31
Carassius auratus	21	-	10	31
Opsariichthys uncirostris	14	-	10	24
Squalidus gracilis majimae	20	-	-	20
Culter brevicauda	20	-	-	20
Pseudogobio esocinus	12	5	-	17
Hemibarbus longirostris	-	15	-	15
Cyprinus carpio	6	-	7	13
Acheilognathus rhombeus	5	-	-	5
Sarcocheilichthys variegatus	2	3	-	5
Squalidus japonicus coreanus	4	-	-	4
Acanthorhodeus macropterus	4	-	-	4
Pseudorasbora parva	3	-	-	3
Coreoleuciscus splendidus	-	2	-	2
Sarcocheilichthys nigripinnis	2	-	-	2
Squaliobarbus curriculus	1	-	1	2
Pseudorasbora parva	1	-	-	1
Pseudopungtungia nigra	1	-	-	1
Rhynchocypris oxycephalus	1	-	-	1
Aphyocypris chinensis	1	-	-	1
Cobitis lutheri	-	1	-	1
Plecoglossus altivelis	1	-	-	1
Siluriformes
Leiocassis ussuriensisa	1	-	-	1
Perciformes
Odontobutis platycephala	12	-	-	12
Siniperca scherzeri	2	-	1	3
Coreoperca herzi	2	1	-	3
Total	356	53	42	451

^a Total 451 freshwater fishes of 32 species were examined.

^b 3 localities, ⑧ Okcheon-gun (Gum-gang); ⑨ Goisan-gun (Cheong-cheon); ⑩ Daecheong-ho (Lake).

Table 4.

Fishes^a collected from middle regions (Gyeongsangbuk-do), Korea

Species of fish	No. of fish collected from 7 localities^b
Species of fish	⑪	⑫	⑬	⑭	⑮	⑯	⑰	Total
Cypriniforms
Zacco platypus	21	-	11	26	24	39	37	158
Pungtungia herzi	24	6	11	2	15	14	4	76
Zacco temminckii	25	-	7	-	8	2	9	51
Squalidus gracilis majimae	5	-	-	-	-	28	9	42
Coreoleuciscus splendidus	13	-	17	-	8	-	-	38
Carassius auratus	1	3	-	14	-	1	14	33
Squalidus japonicus coreanus	-	-	-	-	-	-	29	29
Niwaella multifasciata	3	-	10	-	15	-	-	28
Pseudogobio esocinus	-	3	-	12	-	-	1	16
Hemibarbus longirostris	-	-	-	10	-	-	4	14
Acanthorhodeus gracilis	-	2	-	10	-	-	2	14
Acheilognathus signifer	4	-	-	-	2	-	6	12
Cyprinus capio	-	2	-	10	-	-	-	12
Misgurnus anguillicaudatus	8	2	-	-	1	-	-	11
Hemibarbus labeo	-	6	-	3	-	-	1	10
Opsariichthys uncirostris	-	-	-	4	-	-	6	10
Acheilognathus yamatsutae	-	-	-	-	-	-	9	9
Pseudobagrus fulvidraco	-	-	-	9	-	-	-	9
Koreocobitis naktongensis	-	-	8	-	-	-	-	8
Tribolodon hakonensis	-	-	-	-	-	6	-	6
Pseudobagrus koreanus	-	3	-	2	-	-	-	5
Microphysogobio koreensis	-	-	1	-	2	-	-	3
iksookimia yongdokensis	-	-	-	-	-	3	-	3
Culter brevicauda	-	-	-	2	-	-	-	2
Squalidus chankaensis tsuchigae	-	-	-	-	1	-	-	1
Ladislabia taczanowskii	-	-	-	2	-	-	-	2
Pseudorasbora parva	-	-	-	-	-	-	1	1
Cobitis sinensis	-	-	-	-	-	-	1	1
Osmeriformes
Plecoglossus altivelis	-	-	-	-	-	10	-	10
Siluriformes
Liobagrus andersoni	-	-	15	-	-	-	-	15
Liobagrus obesus	-	-	10	-	1	-	-	11
Silurus microdorsalis	1	-	-	8	-	-	-	9
Perciformes
Coreoperca herzi	6	10	6	11	6	-	3	42
Siniperca scherzer	-	1	-	1	-	-	-	2
Odontobutis platycephala	7	7	1	5	3	-	-	23
Total	118	45	97	131	86	103	136	716

^a Total 716 freshwater fishes in 35 species were examined.

^b ⑪ Ahndong-si; ⑫ Sangju-si; ⑬ Bonghwa-gun; ⑭ Yecheon-gun; ⑮ Youngyang-gun; ⑯ Youngdeok-gun; ⑰ Gunwi-gun.

Table 5.

Fishes^a collected from southern regions (Jeollanam-do), Korea

Species of fish	No. of fish collected from 6 localities^b
Species of fish	⑱	⑲	⑳	㉑	㉒	㉓	Total
Cypriniforms
Zacco platypus	42	1	20	10	10	1	84
Carassius auratus	13	7	10	-	2	2	34
Squalidus chankaensis tsuchigae	4	25	-	-	-	-	29
Acheilognathus yamatsutae	12	7	3	2	-	3	27
Pungtungia herzi	12	1	-	6	3	2	24
Pseudogobio esocinus	8	3	3	3	3	2	22
Liobagrus mediadiposalis	21	-	-	-	-	-	21
Acheilognathus lanceolatus	-	1	8	-	10	-	19
Zacco temminckii	8	-	-	1	10	-	19
Sarcocheilichthys variegatus	4	-	-	15	-	-	19
Coreoleuciscus splendidus	17	1	-	-	-	-	18
Acanthorhodeus macropterus	-	-	-	8	10	-	18
Hemibarbus longirostris	2	6	4	3	-	-	15
Squalidus japonicus coreanus	12	-	1	-	-	-	13
Hemibarbus labeo	3	-	8	-	-	-	11
Sarcocheilichthys nigripinis	-	10	-	-	-	-	10
Opsariichthys uncirostris	3	-	2	-	-	1	6
Hemiculter eigenmanni	5	-	-	-	-	-	5
Acheilognathus majusculus	4	-	-	-	-	-	4
Abbottina springeri	3	-	-	-	-	-	3
Gnathopogon strigatus	-	-	-	3	-	-	3
Rhodeus ocellatus	-	-	-	-	3	-	3
Cobitis lutheri	-	-	-	-	-	3	3
Ladislabia taczanowskii	2	-	-	-	-	-	2
Microphysogobio koreensis	-	2	-	-	-	-	2
Pseudorasbora parva	-	-	-	1	-	-	1
Cyprinus capio	1	-	-	-	-	-	1
Misgurnus anguillicaudatus	-	-	-	-	-	1	1
Microphysogobio longidorsalis	-	1	-	-	-	-	1
Osmeriformes
Plecoglossus altivelis	-	2	-	6	-	-	8
Siluriformes
Liobagrus mediadiposalis	-	-	-	-	-	1	1
Perciformes
Coreoperca herzi	7	-	-	-	-	-	7
Siniperca scherzeri	5	1	-	-	-	-	6
Micropterus salmoides	-	-	5	-	-	-	5
Odontobutis platycephala	3	-	1	-	1	2	7
Total	191	68	65	58	52	18	452

^a Total 452 freshwater fishes of 35 species were examined;

^b ⑱ Gokseong-gun (Seomjin-gang); ⑲ Gurye-gun (Seomjin-gang); ⑳ Naju-si (Youngsan-gang); ㉑Gangjin-gun (Tamjin-gang); ㉒ Jangheung-gun (Tamjin-gang);㉓Boseong-gun (Boseong-gang).

Table 6.

Fishes^a collected from southern regions (Ulsan Metropolitan City and Gyeongsangnam-do), Korea

Species of fish	No. of fish collected from 3 localities^b
Species of fish	㉔	㉕-1	㉕-2	㉕-3	Total
Cypriniforms
Pungtungia herzi	-	24	44	78	146
Zacco platypus	60	21	19	44	144
Pseudogobio esocinus	-	34	16	60	110
Zacco temminckii	4	34	20	32	90
Carassius auratus	5	36	13	18	72
Hemibarbus longirostris	-	31	15	22	68
Acheilognathus majuscules	-	25	13	10	48
Squalidus chankaensis tsuchigae	25	7	2	3	37
Acanthorhodeus macropterus	-	15	-	15	30
Squalidus gracilis coreanus	-	-	2	9	11
Pseudorasbora parva	5	-	-	1	6
Acheilognathus signifer	-	-	6	-	6
Hemibarbus labeo	5	-	-	-	5
Acheilognathus rhombeus	-	3	-	2	5
Acheilognathus koreensis	-	-	4	-	4
Culter brevicauda	-	-	4	-	4
Sarcocheilichthys variegates	-	-	2	2	4
Hemiculter eigenmanni	2	-	2	-	4
Opsariichthys uncirostris	3	-	-	-	3
Pseudobagrus koreanus	-	2	-	-	2
Sarcocheilichthys nigripinnis	-	-	1	-	1
Perciformes
Coreoperca herzi	2	19	8	30	59
Siniperca scherzeri	-	2	-	-	2
Odontobutis platycephala	8	8	8	24	48
Total	119	261	179	350	909

^a Total 909 freshwater fishes of 24 species were examined;

^b ㉔ Ulsan Metropolitan City (Taehwa-gang); ㉕-1 Sancheong-gun (Yangcheon-gang, 2006); ㉕-2 Sancheong-gun (Yangcheon-gang, 2007); ㉕-3 Sancheong-gun (Yangcheon-gang, 2010).

Table 7.

Prevalence and density of C. sinensis metacercariae in fishes from Chungcheongbuk-do, a middle region of Korea

Location and fish sp.	No. of fish examined	No. (%) of fish infected	No. of metacercariae detected
Location and fish sp.	No. of fish examined	No. (%) of fish infected	Total	Range	Average
⑧ Gum-gang (River)
Sarcocheilichthys nigripinnis	2	1 (50.0)	20	-	20.0
Pungtungia herzi	25	1 (4.0)	2	-	2.0
Squalidus gracilis majimae	20	8 (40.0)	15	1-4	1.9
Acanthorhodeus gracilis	41	4 (9.8)	5	1-2	1.3
Acheilognathus ianceolatus	49	3 (6.1)	3	-	1.0
Hemibarbus labeo	34	1 (2.9)	1	-	1.0
Hemiculter eigenmanni	28	1 (3.6)	1	-	1.0
Sarcocheilichthys varbgatus	2	1 (50.0)	1	-	1.0
Pseudopungtungia nigra	1	1 (100)	1	-	1.0
Rhynchocypris oxycephalus	1	1 (100)	1	-	1.0
Subtotal	203	22 (10.8)	50	1-20	2.3
⑨ Cheong-cheon (Stream) in Goisan-gun
Pungtungia herzi	6	4 (66.7)	23	2-12	5.8
Zacco platypus	20	1 (5.0)	3	-	3.0
Sarcocheilichthys varbgatus	3	1 (33.3)	1	-	1.0
Subtotal	29	6 (20.7)	27	1-12	4.5
Total	232	28 (12.1)	77	1-20	2.8

Table 8.

Prevalence and density of C. sinensis metacercariae in fishes from Nakdong-gang, Gyeongsangbuk-do, a middle region of Korea

Location and fish sp.	No. of fish examined	No. (%) of fish infected	No. of metacercariae detected
Location and fish sp.	No. of fish examined	No. (%) of fish infected	Total	Range	Average
⑭ Yecheon-gun
Ladislabia taczanowskii	2	2 (100)	33	5-28	16.5
Culter brevicauda	2	2 (100)	19	2-17	9.5
Pungtungia herzi	2	1 (50.0)	8	-	8.0
Zacco platypus	26	1 (3.8)	4	-	4.0
Pseudogobio esocinus	12	1 (8.3)	1	-	1.0
Hemibarbus longirostris	10	1 (10.0)	2	-	2.0
Hemibarbus labeo	3	1 (33.3)	1	-	1.0
Subtotal	57	9 (15.8)	68	1-28	7.6
⑮ Youngyang-gun
Pungtungia herzi	15	15 (100)	3,736	13-630	249.1
Squalidus chankaensis tsuchigae	1	1 (100)	56	-	56.0
Microphysogobio koeensis	2	2 (100)	54	1-53	27.0
Coreoleuciscus splendidus	8	7 (87.5)	45	1-16	6.4
Acheilognathus signifer	2	1 (50.0)	4	-	4.0
Zacco platypus	24	5 (20.8)	13	1-6	2.6
Subtotal	52	31 (59.6)	3,908	1-630	126.1
⑰ Gunwi-gun
Pseudogobio esocinus	1	1 (100)	2,105	-	2,105
Squalidus gracills majimae	9	9 (100)	7,463	385-1,875	829.2
Pungtungia herzi	4	4 (100)	3,279	329-1,180	819.8
Squalidus japonicus coreanus	29	29 (100)	6,872	9-875	237.0
Acanthorhodeus gracilis	2	2 (100)	136	54-82	68.0
Zacco platypus	37	9 (24.3)	126	1-77	14.0
Pseudorasbora parva	1	1 (100)	11	-	11.0
Hemibarbus longirostris	4	4 (100)	34	3-13	8.5
Acheilognathus signifer	6	6 (100)	43	2-11	7.2
Zacco temminckii	9	1 (11.1)	3	-	3.0
Acheilognathus yamatsutae	9	1 (11.1)	2	-	2.0
Opsariichthys uncirostris	6	1 (16.7)	1	-	1.0
Coreoperca herzi	3	1 (33.3)	1	-	1.0
Hemibarbus labeo	1	1 (100)	1	-	1.0
Subtotal	111	70 (63.1)	20,077	1-2,105	286.8
Total	220	110 (50.0)	24,053	1-2,105	218.7

Table 9.

Prevalence and density of C. sinensis metacercariae in fishes from Seomjin-gang (River), Jeollanam-do, a southern region of Korea

Location and fish sp.	No. of fish examined	No. (%) of fish infected	No. of metacercariae detected
Location and fish sp.	No. of fish examined	No. (%) of fish infected	Total	Range	Average
⑱ Gokseong-gun
Ladislabia taczanowskii	2	2 (100)	604	259-345	302.0
Sarcocheilichthys varbgatus	4	2 (50.0)	379	20-359	189.5
Zacco platypus	42	1 (2.4)	118	-	118.0
Pungtungia herzi	12	10 (83.3)	1,139	1-275	113.9
Squalidus japonicus coreanus	12	3 (25.0)	164	20-93	54.7
Abbottina springeri	3	2 (66.7)	27	2-25	13.5
Squalidus chankaensis	4	3 (75.0)	31	4-16	10.3
Hemibarbus longirostris	2	2 (100)	7	2-5	3.5
Cyprinus capio	1	1 (100)	2	-	2.0
Acheilognathus majusculus	4	2 (50.0)	4	-	2.0
Coreoleuciscus splendidus	17	11 (64.7)	18	1-3	1.6
Carassius auratus	13	1 (7.7)	1	-	1.0
Hemibarbus labeo	3	2 (66.7)	2	-	1.0
Subtotal	119	42 (35.3)	2,496	1-359	59.4
⑲ Gurye-gun
Pungtungia herzi	1	1 (100)	377	-	377.0
Squalidus chankaensis tsuchigae	25	19 (76.0)	771	1-351	40.6
Sarcocheilichthys nigripinis	10	10 (100)	217	6-62	21.7
Microphysogobio koreensis	2	1 (50.0)	14	-	14.0
Siniperca scherzeri	1	1 (100)	4	-	4.0
Hemibarbus longirostris	6	1 (16.7)	3	-	3.0
Pseudogobio esocinus	3	2 (66.7)	2	-	1.0
Acheilognathus yamatsutae	7	1 (14.3)	1	-	1.0
Microphysogobio longidorsalis	1	1 (100)	1	-	1.0
Subtotal	56	37 (66.1)	1,390	1-377	37.6
Total	175	79 (45.1)	3,886	1-377	49.2

Table 10.

Prevalence and density of C. sinensis metacercariae in fishes from rivers in Jeollanam-do, southern regions of Korea

Location and fish sp.	No. of fish examined	No. (%) of fish infected	No. of metacercariae detected
Location and fish sp.	No. of fish examined	No. (%) of fish infected	Total	Range	Average
⑳ Youngsan-gang in Naju-si
Squalidus japonicus coreanus	1	1 (100)	815	-	815.0
Acheilognathus lanceolatus	5	5 (100)	730	2-460	146.0
Hemibarbus longirostris	4	4 (100)	215	23-107	53.8
Opsarichthys uncirostris	2	1 (50.0)	28	-	28.0
Pseudogobio esocinus	3	3 (100)	24	1-12	8.0
Acheilognathus yamatsutae	3	2 (66.7)	10	1-9	5.0
Zacco platypus	20	1 (5.0)	2	-	2.0
Hemibarbus labeo	8	5 (62.5)	6	1-2	1.2
Carassius auratus	10	1 (10.0)	1	-	1.0
Subtotal	56	23 (41.1)	1,831	1-460	79.6
㉑ Tamjin-gang in Gangjin-gun
Pungtungia herzi	6	6 (100)	2,520	95-846	420.0
Sarcocheilichthys varbgatus	15	15 (100)	5,342	65-682	356.1
Gnathopogon strigatus	3	3 (100)	122	30-52	40.7
Pseudorasbora parva	1	1 (100)	6	-	6.0
Acanthorhodeus macropterus	8	5 (62.5)	14	1-9	2.8
Pseudogobio esocinus	3	3 (100)	6	1-3	2.0
Acheilognathus yamatsutae	2	2 (100)	4	1-3	2.0
Hemibarbus longirostris	3	3 (100)	5	1-3	1.7
Zacco platypus	10	1 (10.0)	1	-	1.0
Subtotal	51	39 (76.5)	8,020	1-846	205.6
㉓ Boseong-gang in Boseong-gun
Pungtungia herzi	2	2 (100)	157	9-148	78.5
Pseudogobio esocinus	2	1 (50.0)	2	-	2.0
Acheilognathus yamatsutae	3	1 (33.3)	2	-	2.0
Zacco platypus	1	1 (100)	1	-	1.0
Subtotal	8	5 (62.5)	162	1-148	32.4
Total	115	67 (58.3)	10,013	1-846	149.4

Table 11

Prevalence and density of C. sinensis metacercariae in fishes from Yangcheon-gang (River), Sancheong-gun, Gyeongsangnam-do, a southern region of Korea

Year examined and fish sp.	No. of fish examined	No. (%) of fish infected	No. of metacercariae detected
Year examined and fish sp.	No. of fish examined	No. (%) of fish infected	Total	Range	Average
2006
Pungtungia herzi	24	24 (100)	19,044	324-1,408	793.5
Squalidus chankaensis tsuchigae	7	7 (100)	1,775	100-380	253.6
Pseudogobio esocinus	34	34 (100)	3,643	2-313	107.2
Acheilognathus rhombeus	3	3 (100)	187	37-112	62.3
Acanthorhodeus macropterus	15	10 (66.7)	335	1-83	33.5
Acheilognathus majuscules	25	18 (72.0)	100	1-44	5.6
Hemibarbus longirostris	31	7 (22.6)	13	1-3	1.9
Zacco temminckii	34	4 (11.8)	6	1-3	1.5
Zacco platypus	21	3 (14.3)	3	-	1.0
Subtotal	194	110 (56.7)	25,106	1-1,408	228.2
2007
Pungtungia herzi	44	44 (100)	28,294	106-2,345	707.4
Squalidus chankaensis tsuchigae	2	2 (100)	658	178-480	329.0
Sarcocheilichthys varbgatus	2	2 (100)	551	145-406	275.5
Squalidus gracilis coreanus	2	2 (100)	298	89-209	149.0
Pseudogobio esocinus	16	13 (81.3)	817	1-197	62.9
Sarcocheilichthys nigripinnis	1	1 (100)	11	-	11.0
Hemiculter eigenmmni	2	2 (100)	14	-	7.0
Acheilognathus signifer	6	6 (100)	35	1-16	5.8
Coreoperca herzi	8	1 (12.5)	4	-	4.0
Hemibarbus longirostris	15	8 (53.3)	23	1-10	2.9
Zacco platypus	19	1 (5.3)	2	-	2.0
Acheilognathus koreensis	4	2 (50.0)	4	1-3	2.0
Acheilognathus majusculus	13	9 (69.2)	16	1-4	1.8
Carassius auratus	13	1 (7.7)	1	-	1.0
Odontobutis platycephala	8	1 (12.5)	1	-	1.0
Subtotal	155	95 (61.3)	30,729	1-2,345	323.4
2010
Sarcocheilichthys varbgatus	2	2 (100)	542	240-302	271.0
Pungtungia herzi	78	71 (91.0)	13,143	1-1,286	185.1
Squalidus chankaensis tsuchigae	3	3 (100)	235	48-131	78.3
Pseudorasbora parva	1	1 (100)	45	-	45.0
Acheilognathus rhombeus	2	2 (100)	51	15-36	25.5
Squalidus gracilis coreanus	9	8 (88.9)	191	2-59	23.9
Acheilognathus macropterus	15	11 (73.3)	263	4-98	23.9
Pseudogobio esocinus	60	55 (91.7)	994	1-136	18.1
Zacco platypus	44	5 (11.4)	12	1-8	2.4
Hemibarbus longirostris	22	17 (77.3)	37	1-6	2.2
Acheilognathus majusculus	10	1 (10.0)	1	-	1.0
Subtotal	246	176 (71.5)	15,514	1-1,286	88.1
Total	595	381 (64.0)	71,349	1-2,345	187.3

Table 12.

Comparative prevalence^a and density^a of C. sinensis metacercariae in fishes from 3 latitudinal regions

Items	Infection status (%) in fishes from
Items	Northern	Middle	Southern	Total
No. (%) of fish examined	1,543 (37.9)	1,167 (28.7)	1,361 (33.4)	4,071 (100)
Total positive rate (%)	11/1,543 (0.7)	149/1,167 (12.8)	538/1,361 (39.5)	698/4,071 (17.1)
Overall metacercarial density/fish	2.6	163.7	158.8	157.4
Positive rate (%) of P. herzi	9/146 (6.2)	34/107 (31.8)	158/170 (92.9)	201/423 (47.5)
Metacercarial density in P. herzi	2.8	214.7	409.3	358.2
Positive rate (%) of Z. platypus	0/247 (0)	17/223 (7.6)	13/228 (5.7)	30/698 (4.3)
Metacercarial density in Z. platypus	0	8.6	10.7	9.5

^a Prevalence: no. of fish infected/no. of fish examined×100; density: mean no. of metacercariae per infected fish.