Infection Status with Metagonimus spp. Metacercariae in Fishes from Seomjin-gang and Tamjin-gang in Republic of Korea

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Abstract

INTRODUCTION

Members in the genus Metagonimus Katsurada, 1912 (Digenea: Heterophyidae) are comprised more than 7 nominal species, i.e., M. yokogawai Katsurada, 1912, M. takahashii Suzuki, 1930, M. minutus Katsuta, 1932, M. katsuradai Izumi, 1935, M. otsurui Saito and Shimizu, 1968, M. miyatai Saito et al., 1997 and M. hakubensis Shimazu, 1999. Among 7 Metagonimus species, 3 ones, i.e., M. yokogawai, M. takahashii, and M. miyatai, are known to distribute in the Republic of Korea (Korea) [1,2]. Human infection by these species of fluke, metagonimiasis, is an important endemic disease together with clonorchiasis in Korea [1–3]. Infections by M. yokogawai are chiefly prevalent in the riverside areas of eastern and southern coast of Korean peninsula [3–7]. Human cases by M. takahashii were first reported in inhabitants of Eumseong-gun (gun=county), Chungcheongnam-do (do=Province), along the upper reaches of the Namhan-gang [6]. Endemic areas of M. miyatai were confirmed among peoples residing around lakes and along the rivers and/or streams in inland of Korea [9–11]. These Metagonimus species give rise to severe gastrointestinal troubles and chronic diarrhea in heavily infected cases [1,2,12].

As the infection sources of metagonimiasis, lots of fish species have been reported in Korea [13]. The sweet smelt (Plecoglossus altivelis), the sea rundace (Tribolodon hakonensis) and the Japanese seabass (Lateolabrax japonicus), are known to be the second intermediate hosts of M. yokogawai [13–16]. The crusian carp (Carassius auratus), common carp (Cyprinus carpio), sea rundace, and Japanese seabass are reported as the second intermediate hosts of M. takahashii [13,16,17]. As the second intermediate hosts of M. miyatai, many species of fish, including the sea rundace, pale chub, (Zacco platypus) and dark chub (Z. temminckii), are listed in Korea [13,16,18].

On the other hand, many Korean workers have been investigated the infection status with zoonotic trematodes (ZT), i.e., C. sinensis, Metagonimus spp. including M. yokogawai, Centrocestus armatus and Echinostoma spp., metacercariae in fishes from various endemic areas to estimate the endemicities of these trematode infections [1,13]. In case of Metagonimus spp., most of studies were performed on the infection status of M. yokogawai in sweet smelts from the specific regions [19–25]. Recently, Cho et al. [26] surveyed on the infection status of ZT metacercariae including Metagonimus spp. in freshwater fish from Gangwon-do, Korea. Sohn et al. [27] investigated the infection status of digenetic trematode metacercariae in freshwater fish from the water systems of Hantan-gang and Imjin-gang located in relatively northern regions of Korea. Sohn et al. [28] and Yoon et al. [29] reported the infection status with C. sinensis metacercariae in fishes from Seomjin-gang and Tamjin-gang. However, the infection status with MsMc in fish from Seomjin-gang and Tamjin-gang has not been widely and systematically examined yet, although these 2 riverside areas has been known as the endemic areas of heterophyid flukes including M. yokogawai [3,4,30–32]. Therefore, we performed the present study to know the infection status with MsMc in fishes from 2 rivers, Seomjingang and Tamjin-gang, located in the southern parts of Korea.

MATERIALS AND METHODS

Fishes examined in the upper reaches of Seomjin-gang

Total 236 freshwater fish (11 species) from Osucheon in Imsil-gun, Jeollabuk-do were examined in 2012 and 2013. Fish species (No. of fish) examined were Squalidus japonicus coreanus (20), Microphysogobio jeoni (6), Pseudogobio esocinus (5), Carassius auratus (3), and Hemibarbus longirostris (1) including 6 ones with MsMc in Table 1. Total 310 freshwater fish (29 species) from Seomjin-gang in Sunchang-gun, Jeollabuk-do were examined in 2014 and 2015. Fish species (No. of fish) examined were Coreoperca herzi (19), Acheilognathus koreensis (12), Odontobutis platycephala (9), Coreoleuciscus splendidus (4), Acheilognathus yamatsutae (3), Abbottina springeri (3), Cobitis tetralineata (2), Acheilognathus lanceolatus (1), Acanthorhodeus macropterus (1), Cobitis lutheri (1), and Misgurnus anguillicaudatus (1) including 18 ones with MsMc in Table 1.

Table 1

Infection status of Metagonimus spp. metacercariae in freshwater fish from the upper reaches of Seomjin-gang (River)

Fishes examined in the middle reaches of Seomjingang

Total 196 freshwater fish (14 species) from Songdaecheon in Namwon-si, Jeollabuk-do were examined in 2012 and 2013. Fish species (No. of fish) examined were C. herzi (6), Pseudorasbora parva (2), A. springeri (2), P. esocinus (1), Iksookimia longicorpus (1), and Lepomis macrochirus (1) including 8 ones with MsMc in Table 2. Total 289 freshwater fish (15 species) from Seomjin-gang in Gokseong-gun, Jeollanam-do were examined in 2015 and 2016. Fish species (No. of fish) examined were Ladislabia taczanowskii (1) including 14 ones with MsMc in Table 2.

Table 2

Infection status of Metagonimus spp. metacercariae in freshwater fish from the middle reaches of Seomjin-gang (River)

Fishes examined in the lower reaches of Seomjin-gang

Total 183 freshwater fish (21 species) from Seomjin-gang in Gurye-gun, Jeollanam-do were examined in 2014. Fish species (No. of fish) examined were C. auratus (5), O. platycephala (4), A. lanceolatus (3), and S. scherzeri (1) including 17 ones with MsMc in Table 3. Total 156 freshwater fish (13 species) from Hoengcheon in Hadong-gun, Gyeongsangnam-do were examined in 2014 and 2016. Fish species (No. of fish) examined were C. auratus (1) and O. platycephala (1) including 11 ones with MsMc in Table 3. Total 234 freshwater fish (12 species) from Namsancheon in Hadong-gun, Gyeongsangnam-do were examined in 2015 and 2016. Fish species (No. of fish) examined were C. auratus (16), A. koreensis (7), A. gracilis (2), C. splendidus (1), and O. platycephala (1) including 7 ones with MsMc in Table 3.

Table 3

Infection status of Metagonimus spp. metacercariae in freshwater fish from the lower reaches of Seomjin-gang (River)

Fishes examined in Tamjin-gang

In the middle reaches in Jangheung-gun, total 1,132 fishes in 22 species were examined for 4 years (2014–2017). Fish species (No. of fish) examined were Micropterus salmoides (8), A. koreensis (7), and Cyprinus carpio (2) including 19 ones with MsMc in Table 5. In the lower reaches in Gangjin-gun, a total of 517 fishes in 17 species were examined in 2014 and 2017. Fish species (No. of fish) examined were A. lanceolatus (22), C. herzi (3), and Mugil cephalus (1) including 14 ones with MsMc in Table 5.

Table 5

Infection status of Metagonimus spp. metacercariae in fishes from Tamjin-gang (River) in Jeollanam-do, Korea

RESULTS

Infection status with MsMc in rasborinid fish from Seomjin-gang

MsMc were detected in 547 (89.2%) out of total 613 rasborinid fishes from Seomjin-gang, and their average density was 73.6 per fish infected. The infection status by the rasborinid fish species and surveyed reaches of river was detailedly revealed in Table 4.

Table 4

Infection status of Metagonimus spp. metacercariae in rasborinid fish from Seomjin-gang (River)

Infection status with MsMc in the susceptible fish species from Tamjin-gang

MsMc were detected in 556 (84.1%) out of total 661 susceptible fishes from Tamjin-gang, and their average density was 227 per fish infected. The infection status by the fish species and surveyed areas was detailedly revealed in Table 6.

Table 6

Infection status of Metagonimus spp. metacercariae in susceptible fishes from Tamjin-gang (River) in Jeollanam-do, Korea

DISCUSSION

By the present study, it was confirmed that MsMc are more or less prevalent in fishes from Seomjin-gang and Tamjingang. The positive rates with MsMc were very similar, 55.4% and 59.3%, in fishes from 2 rivers, but average metacercarial densities were 96 and 138 per fish infected, higher in fishes from Tamjin-gang. We couldn’t compare the endemicity of MsMc in the most susceptible fish species, sweet smelt (P. altivelis), so the number of fish examined (8 from Seomjin-gang and 92 from Tamjin-gang) was too much different in 2 rivers. However, their prevalences were 100% and 98.9% and densities were 5,171 and 1,120 per fish infected in sweet smelts from Seomjin-gang and Tamjin-gang each. In another MsMc susceptible fish group, rasborinid fish such as Zacco spp. and O. uncirostris amurensis, the prevalences were very similar, 89.2% and 89.0%, in 2 rivers, but average metacercarial densities were 74 and 42 per fish infected, more or less higher in Seomjin-gang (Table 7). On the other hand, in the rasborinid fish from Seomjin-gang, the prevalences were 72.4% (the upper reaches), 93.5% (the middle reaches), and 98.7% (the lower reaches), and metacercarial densities were 12.6, 38.4, and 137.2 per fish infected respectively. These findings suggested that the endemicity with MsMc is more higher in fish from the lower reaches than in fish from the upper and middle reaches of Seomjin-gang. In the susceptible fish species, i.e., Zacco spp., C. auratus and P. altivelis, from Tamjin-gang, the prevalence was 84.1% (80.1% in the middle reaches and 93.1% in the lower reaches) and MsMc density was 227 (238 in the middle reaches and 205 in the lower reaches) per fish infected. Therefore, the endemicity with MsMc is similar in fish from 2 surveyed sites of Tamjin-gang.

Table 7

Comparison of the infection statusa with Metagonimus spp. metacercariae in fishes from Seomjin-gang and Tamjin-gang

With regard to the infection status of MsMc in sweet smelts, P. altivelis, from Seomjin-gang and Tamjin-gang, at least 4 studies were available [4,21,22,25]. In 1977, Chai et al. [4] reported 100% prevalence and 15,688 MsMc per fish in 20 sweet smelts from a water reservoir nearby Tamjin-gang in Jangheung-gun. Seo et al. [22] detected av. 14,887 MsMc in all 16 sweet smelts from Tamjin-gang in Gangjin-gun. In 1985, Song et al. [21] reported 92.3% prevalence and 636 MsMc per fish in 12 sweet smelts from Tamjin-gang in Gangjin-gun. Cho et al. [25] detected av. 1,037 and 1,511 MsMc per fish in 16 sweet smelts from Tamjin-gang in Gangjin-gun and in 20 ones from Seomjin-gang in Gurye-gun, Jeollanam-do. Song et al. [21] also reported 2,724 and 2,412 MsMc per fish in each 5 sweet smelts from Seomjingang in Gokseong-gun and Gurye-gun, Jeollanam-do. In this study, all 8 sweet smelts from Seomjin-gang were infected with av. 5,171 MsMc, and 91 (98.9%) sweet smelts from Tamgingang were infected with 1,120 MsMc per fish infected. From the above findings of present and previous studies, we can suppose that the sweet smelts naturally produced in 2 rivers are highly infected with MsMc and the riverside areas are to be the highly endemic regions of metagonimiasis.

The rasborinid fish, i.e., Z. platypus, Z. koreanus, Z. temminckii and O. uncirostris amurensis, are known as the susceptible fish hosts of MsMc in both regions without and/or with sweet smelts in Korea. These fish species are also known as the second intermediate hosts of M. miyatai [9,18]. One of them, Z. platypus, is the most dominant species in the water systems of Korea. And then the rasborinid fish, especially Zacco spp., are highly recommended as the index fish of MsMc to evaluate the endemicity of metagonimiasis. In the present study, total 1004 (30.9%) rasborinid fish (613 from Seomjin-gang: 38.2% and 391 from Tamjin-gang: 23.7%) were examined, and 895 (89.1%) ones (547 in Seomjin-gang: 89.2% and 348 in Tamjin-gang: 89.0%) were to be infected with MsMc. Their density was 61.1 per fish infected (73.6 in Seomjin-gang and 41.5 in Tamjin-gang) (Table 7). In the water systems of Gangwon-do, the prevalences with MsMc were 23.5–100% (85.2% in average) in rasborinid fish and their densities were 3.4–108 (29.7 in average) in 10 surveyed areas [26]. Sohn et al. [27] reported 73.9% and 72.1% MsMc prevalences in the rasborinid fish from the water systems of Hantan-gang and Imjin-gang. They also reported av. 43.1 and 18.6 MsMc densities in the rasborinid fish from 2 surveyed areas [27]. From the aforementioned findings, we can suppose that the endemicities with MsMc in fishes from Seomjin-gang and Tamjin-gang are more higher than those from the water systems of Gangwon-do, Hantan-gang and Imjin-gang.

Among fishes from Seomjin-gang, some rasborinid fishes, i.e., Z. koreanus and Z. temminckii from Hoengcheon and Namsancheon in Hadong-gun, O. uncirostris amurensis from Seomjin-gang in Gurye-gun and Z. platypus from Seomjin-gang in Gurye-gun and Hoengcheon in Hadong-gun, were revealed 100% prevalences and more than 100 MsMc densities. In fishes from Tamjin-gang, crusian carp, C. auratus, from Jangheung-gun and dark chub, Z. temminckii, from Gangjin-gun were highly and heavily infected with MsMc. Among fishes from the water systems of Gangwon-do, 90.0% sea rundace, T. hakonensis, from Namdaecheon in Yangyang-gun and 97.4% dark chub, Z. temminckii, from Joyang-gang in Jeongseon-gun were infected with 449 and 130 MsMc per fish infected [26]. Sohn et al. [27] reported 92.3% and 100% prevalences and 132 and 102 MsMc densities in 26 P. esocinus and 22 Z. platypus from Hantan-gang in Cheorwon-gun, Gangwon-do. These findings on the high infection status with MsMc will be helpful to perform a study on the experimental metagonimiasis to be needed massive MsMc.

More than 7 valid species have been reported in the genus Metagonimus flukes in the literatures. All of them mainly distributed in Asian countries such as Japan, Korea, China and Taiwan [2]. At least 3 human infecting species, i.e., M. yokogawai, M. takahashii and M. miyatai, are known to exist commonly in Japan and Korea [1,2]. They are morphologically differentiated in adult stage by the locations of uterus and vitellaria, and the size of eggs, but not in metacercarial stages in the fish intermediate hosts. The cercariae of Metagonimus spp. naturally shed from freshwater snails, Semisulcospira coreana and S. libertina, which are known as the first intermediate hosts in Korea, and they penetrate into the second intermediate hosts. As the second intermediate hosts of Metagonimus spp., numerous species of fish have been reported in Korea. However, some fish species are known as hosts of specific Metagonimus species, i.e., P. altivelis, T. hakonensis and L. japonicus for M. yokogawai [13–16]; C. auratus, C. carpio, T. hakonensis and L. japonicus for M. takahashii [13,16,17]; Z. platypus and Z. temminckii for M. miyatai [13,18]. Does each species of Metagonimus spp. cercariae have the host-specificity? How does each species of cercariae encyst in the favorable fish hosts only in even highly endemic environment like Seomjin-gang and Tamjin-gang? Studies on the host-specificity of each Metagonimus sp. in fish hosts should be clarified in the near future through the morphological analysis of adult worms recovered from experimental animals, which are infected with MsMc from some susceptible species of fish, i.e., sweet smelt, sea rundace, crusian carp, pale chub and dark chub from a same endemic area.

Conclusively, by the present study, it was confirmed that MsMc are more prevalent in fishes from Seomjin-gang and Tamjin-gang than from any other rivers in Korea. Peoples residing in riverside areas of the 2 rivers should pay attention to the raw consumption of the susceptible fish hosts like chubs, Zacco spp., and crusian carp, C. auratus as well as sweet smelt, P. altivelis.

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