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Fishborne Trematode Metacercariae in Freshwater Fish from Guangxi Zhuang Autonomous Region, China
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Original Article

Fishborne Trematode Metacercariae in Freshwater Fish from Guangxi Zhuang Autonomous Region, China

Woon-Mok Sohn1, Keeseon S. Eom2, Duk-Young Min3, Han-Jong Rim4, Eui-Hyug Hoang5, Yichao Yang6, Xueming Li6
The Korean Journal of Parasitology 2009;47(3):249-257.
Published online: August 28, 2009

1Department of Parasitology and Institute of Health Sciences, Gyeongsang National University School of Medicine, Jinju 660-751, Korea.

2Department of Parasitology and Medical Research Institute, Chungbuk National University School of Medicine, Cheongju 360-763, Korea.

3Department of Parasitology, Hanyang University College of Medicine, Seoul 133-791, Korea.

4Department of Parasitology, College of Medicine, Korea University, Seoul 136-705, Korea.

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Corresponding author (wmsohn@gnu.ac.kr)
• Received: April 6, 2009   • Revised: May 16, 2009   • Accepted: June 5, 2009

Copyright © 2009 by The Korean Society for Parasitology

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  • A survey was performed to investigate the infection status of fishborne trematode (FBT) metacercariae in freshwater fish from Guangxi Zhuang Autonomous Region, China. A total of 307 freshwater fish of 31 species were collected from 5 administrative regions of Guangxi Zhuang Autonomous Region. They were examined by artificial digestion method from July 2003 to August 2004. No metacercariae were detected in fish from Fusui-xian. In fish from Mashan-xian and a market in Nanning, 3 species of metacercariae, Haplorchis taichui, Haplorchis pumilio, and Centrocestus formosanus, were mainly detected. Metacercariae (8 in number) of Clonorchis sinensis were found in 1 Chanodichthys dabryi purchased from a market in Nanning. In fish from Yangshuo, Metagonimus yokogawai metacercariae were detected from all 18 fish species examined. Total 13 C. sinensis metacercariae were found in 3 out of 10 Hemibarbus maculatus from Yangshuo. All 7 Zacco platypus from Yangshuo were infected with 8-112 Echinochasmus perfoliatus metacercariae. In fish from Binyang-xian, H. pumilo metacercariae were mainly detected in all 5 fish species examined, and only 1 metacercaria of C. sinensis was found in a Hemiculter leucisculus. From the above results, it was confirmed that some species of freshwater fish play a role of second intermediate hosts for FBT in Guangxi Zhuang Autonomous Region, China. In particular, 4 species of intestinal flukes, M. yokogawai, H. taichui, H. pumilio, and C. formosanus, were prevalent in fish hosts, whereas C. sinensis metacercariae were detected only in 3 fish species.
  • Key words: Haplorchis taichui, Haplorchis pumilio, Centrocestus formosanus, Metagonimus yokogawai, Clonorchis sinensis, fishborne trematode metacercariae, freshwater fish, Guangxi Zhuang Autonomous Region, China
Fishborne trematode (FBT) infections affect the health of more than 18 million people around the world, particularly in Asian countries. These flukes provoke remarkable morbidity and cause serious damage to aquaculture in developing countries [1,2]. The liver flukes, Clonorchis sinensis and Opisthorchis spp., have been known as the representative FBT. Many species of intestinal flukes, mainly belonging to the family Heterophyidae and Echinostomatidae are also infected by eating raw fish [2].
In the Republic of Korea, many species of FBT including C. sinensis have been reported. C. sinensis is still prevalent in riverside areas and is the most important helminth species of public health importance. About 10 species of the Heterophyidae and 3 of the Echinostomatidae have been reported as the intestinal flukes infected by eating raw fish meat [3-6]. On the other hand, C. sinensis infections are found in 22 out of 30 PRM (Province/Autonomous Region/Municipality) in China. Especially, prevalences in 4 provinces, Guangdong, Guangxi, Anhui and Heilongjiang, are much higher than those of the other regions [7-9]. As the intestinal FBT, 8 species of the Heterophyidae (Metagonimus yokogawai, M. takahashii, Stellantchasmus falcatus, Centrocestus formosanus, Haplorchis pumilio, H. taichui, and H. yokogawai) and 5 species of the Echinostomatidae (Echinostoma angustitestis, Echinochasmus japonicus, E. perfoliatus, E. liliputanus, and E. fujianensis) are distributed in China [10].
Guangxi Zhuang Autonomous Region (GZAR) locates in the southern part of China, on the subtropical zone and its southwest area contact with Vietnam. This province has many minority people. They have some different food habit. Some monority people like to eat raw fish and easily infect with FBT. Furthermore, they have engaged in aquaculture in the fishponds with latrines that contribute as an important source of contamination [11]. It has been revealed that many minority peoples are infected with FBT including C. sinensis in GZAR, China [11]. However, the major source of infection has not yet been obvious. Therefore, we performed epidemiological surveys to know the second intermediate hosts and the infection status of FBT metacercariae in freshwater fish from 5 administrative regions of GZAR, China.
A total of 307 freshwater fish of 31 species was collected from 5 administrative regions, Fusui-xian, Mashan-xian, Nanning City, Yangsuo County, and Binyang-xian, in GZAR, China from July 2003 to August 2004 (Table 1). All collected fish were transferred to the laboratories (Division of Helminthiasis Prevention and Control, Guangxi Centre for Disease Prevention and Control, Nanning, China, and Department of Parasitology, Gyeongsang National University School of Medicine, Jinju, Korea), individually measured the length and weight according to the species, and identified the fish species with the aid of ichthyologists in Nanning, GZAR, China, and FishBase site in internet [12]. They all were finely ground with a mortar with pestle or a grinder. The 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 were separately collected by the general feature, and they were identified species level based on the detail morphologies and their demensions under a light microscope. Identified metacercariae were experimentally infected to mice, rats, hamsters, chicks and cats to obtain adult worms.
Infection status in fish from Fusui-xian and Mashan-xian
No metacercariae were detected in fish from Fusui-xian. However, in fish from Mashan-xian, 3 species of metacercariae, H. taichui, H. pumilio, and C. formosanus, were detected. H. taichui metacercariae were found in 7 fish species and their infection status is presented in Table 2. H. pumilio metacercariae were detected in 10 fish species. Among them, Opsariichthys bidens, Puntius semifasciolatus, Pseudohemiculter dispar, and Carassius auratus were heavily infected (Table 3). C. formosanus metacercariae were found in 3 fish species. Especially, Microphysogobio fukiensis was infected with more than 300 metacercariae of C. formosanus (Table 4).
Infection status in fish from Nanning City
In freshwater fish from a market in Nanning, 3 species of metacercariae, H. taichui, H. pumilio, and C. formosanus, were mainly detected. H. taichui metacercariae were found in 11 fish species. Among them, Hemiculter leucisculus, Toxabramis houdemeri, and Cyprinus carpio were heavily infected with H. taichui metacercariae (Table 5). H. pumilio metacercariae were detected in 11 fish species, and their infection status is shown in Table 6. C. formosanus metacercariae were found in 7 fish species and their infection status is shown in Table 7. One Chanodichthys dabryi was infected with 3 metacercariae of C. sinensis. Four metacercariae of Metagonimus sp. were detected in 1 Hemibarbus maculatus.
Infection status in fish from Yangshuo County
In freshwater fish from Yangshuo, Metagonimus sp. metacercariae were detected from all 18 fish species examined. Among them, Zacco platypus, H. maculatus, P. semifasciolatus, and Abbottina rivularis were infected with more than 100 metacercariae per infected fish (Table 8). A total of 13 C. sinensis metacercariae were found in 3 out of 10 Hemibarbus maculatus examined. All 7 Z. platypus examined were infected with 8-112 metacercariae of E. perfoliatus.
Infection status in fish from Binyang-xian
In freshwater fish from Binyang-xian, H. pumilo metacercariae were mainly detected in all 5 fish species examined, and their infection status is presented in Table 9. Metorchis taiwanensis metacercariae were found in 4 Ctenopharyngodon idella (40%) and their numbers were ranged in 1-425. Only 1 metacercaria of C. sinensis was detected in H. leucisculus.
Overall infection status of fish from GZAR, China
Metacercariae of Metagonimus sp. were detected in 18 species of fish, and their fish hosts are revealed in Table 8 (see full names of fish). Those of H. taichui were found in 15 fish species, such as H. molitrix, C. auratus, H. maculatus, T. houdemeri, P. dispar, O. bidens, S. argentatus, C. carpio, A. rivularis, P. semifasciolatus, H. leucisculus, C. recurviceps, S. dabryi, M. lineate, and C. dabryi. H. pumilio metacercariae were detected in 18 fish species, i.e., C. auratus, A. tonkinensis, H. maculatus, H. molitrix, H. leucisculus, C. idella, T. houdemeri, M. fukiensis, P. dispar, O. bidens, S. argentatus, M. lineata, C. carpio, P. semifasciolatus, S. dabryi, C. recurviceps, C. dabryi, and P. parva. C. formosanus metacercariae were found in 10 fish species, such as M. fukiensis, A. tonkinensis, S. argentatus, C. carpio, H. molitrix, A. rivularis, H. leucisculus, M. lineata, S. dabryi, and P. parva (Table 10). On the other hand, metacercariae of C. sinensis were demonstrated in low infection rates and intensities in only 3 fish species, H. maculatus, C. dabryi, and H. leucisculus.
Morphology of metacercariae detected
H. taichui metacercariae (n = 20) were elliptical, 188-220 (203 in average) × 155-185 (168 in average) µm in size, had a baseball glove-shaped ventro-genital sac with 11-18 rodlets and an O-shaped excretory bladder occupying large portion of posterior body (Fig. 1A).
H. pumilio metacercariae (n = 20) were elliptical, 155-188 (172) × 138-163 (152) µm in size, had 36-42 deer horn-like minute spines arranged in 1-2 rows around ventrogenital complex, and an O-shaped excretory bladder occupying large portion of posterior body (Fig. 1B).
C. formosanus metacercariae (n = 30) were elliptical, 173-233 (208) × 135-178 (164) µm in size, had 32 circumoral spines around oral sucker arranged in 2 rows, and a X-shaped excretory bladder occupying greater portion of posterior body (Fig. 2A).
Metagonimus sp. metacercariae (n = 30) were elliptical, 138-200 (154) × 120-183 (144) µm in size, had yellow brownish pigment granules scattering in body area of intestinal bifurcation, a ventral sucker deflectively located from median, and a V-shaped excretory bladder (Fig. 2B).
C. sinensis metacercariae (n = 10) were elliptical, 158-193 (182) × 153-183 (168) µm in size, had 2 nearly equal sized suckers, brownish pigment granules scattering in the body, and an O-shaped excretory bladder occupying greater part of posterior body (Fig. 3A).
E. perfoliatus metacercariae (n = 10) were elliptical, 95-110 (105) × 75-88 (85) µm in size, had a transparent and double layered cyst wall, 24 dorsally interrupted collar spines, and a ventral sucker lying median on posterior 1/3 of body and as large as oral sucker (Fig. 3B).
M. taiwanensis metacercariae (n = 10) were globular, 163-170 (166) × 150-170 (162) µm in size, had a double layered cyst wall (transparent and very thick outer layer: 43-52 µm and inner layer: 5.0-7.5 µm in thickness), 2 nearly equal sized suckers, and an O-shaped excretory bladder (Fig. 4).
Morphological characters of Metagonimus yokogawai adults (n = 20)
Adults of M. yokogawai were recovered from experimentally infected dogs and cats with metacercariae collected from fish from Yangshou county. They were 0.882 × 0.437 mm in average size, had the larger ventral sucker (av. 90 × 66 µm), deviated to right side from median, than oral sucker (av. 51 × 62), muscular pharynx (av. 37 × 32), moderately long esophagus (av. 88) and ceca. The round or elliptical ovary (av. 70 × 77) was located in median portion of body, and 2 adjacent testes (right: av. 139 × 107; left av. 127 × 98) were obliquely situated near the posterior end of body. The uterine loop passed through anterior border of both testis, and the uterine eggs were elliptical, yellow in color, 24.0-26.8 (av. 25.4) long and 15.0-17.5 (av. 15.6) wide (Fig. 5).
World Health Organization (WHO) estimated that more than 18 million people are infected with fishborne trematodes (FBT), and more than half of billion people are at risk of FBT infections around the world [1,13]. FBT infections are classified as zoonoses because they are viewed as animal diseases transmitted to human. Some infections appear to be rare while others are common and cause serious disease. It has been known that liver flukes, C. sinensis and Opisthorchis spp., and some groups of intestinal flukes are representative FBT, and they are mainly infected by eating raw meat of freshwater and estuarine fish in low- and middle-income countries. On the other hand, it has been revealed that so many peoples are infected with FBT including C. sinensis in GZAR, China by the work of "Korea-China Collaborative Project of Control Strategies for Helminthiasis" [11]. However, it has not been obvious that what kinds of fish play a role of second intermediate host of FBT in this area. Therefore, present study was performed to investigate the infection status of FBT metacercariae in freshwater fish from GZAR, China.
Through this study, it was confirmed that some species of FBT metacercariae are prevalent in freshwater fish from GZAR, China. Especially, four species of intestinal flukes, H. taichui, H. pumilio, M. yokogawai and C. formosanus, were prevalent in fish hosts while C. sinensis metacercariae were detected from only 3 species of fish. Besides aforementioned 5 species, E. perfoliatus and M. taiwanensis metacercariae were also found in this study. Moreover, it was proved for the first time that 4 trematode species, H. pumilio, M. yokogawai, E. perfoliatus and M. taiwanensis, are distributed in GZAR, China [10].
About 70 species belonging to the 14 families, i.e., Heterophyidae, Echinostomatidae, Plagiorchiidae, Lecithodendriidae, Neodiplostomidae, Nanophyetidae, Paramphistomatidae, Cathaemaciidae, Fasciolidae, Gastrodiscidae, Gymnophallidae, Microphallidae, Strigeidae and Brachylaimidae, have been found in the intestinal tract of humans around the world. Among members in these families, it has been known that Heterophyidae and Echinostomatidae are the major groups [14]. In China, it has been revealed that Fasciolopsis buski is most important intestinal fluke by the prevalence and morbidity, and 8 species of Heterophyidae (M. yokogawai, M. takahashii, Stellantchasmus falcatus, C. formosanus, H. pumilio, H. taichui and Haplorchis yokogawai) and 5 species of Echinostomatidae (Echinostoma angustitestis, Echinochasmus japonicus, E. perfoliatus, Echinochasmus liliputanus and Echinochasmus fujianensis) are reported as the intestinal FBT [10].
H. taichui metacercariae have been recorded in fish from several Asian countries, i.e. India, Thailand, the Philippines, Lao PDR and China [10, 15-20]. They were detected in 4 fish species, Cirrhinus reba (= Labeo ariza), Amblypharyngodon mola, Labeo bata, and Puntius sophore, in India, 3 fish species, Puntius binotatus, Puntius palata (= Spratellicypris palata), and Ophicephalus striatus (= Channa striata), in the Philippines, 3 fish species, Barbonymus gonionotus, Puntius brevis, and Puntius orphoides, in Thailand, 11 fish species, Hampala dispar, Hampala macrolepidota, B. gonionotus, Mystacoleucus maginatus, P. brevis, Puntioplites falcifer, Cyclocheilchthys armatus, Cyclocheilchthys repasson, Onychostoma elongatum, Labiobarbus leptocheila, and Cirrhnus molitorella, in Lao PDR, and 7 fish species, Carassius auratus, Cyprinus carpio, Ctenopharyngodon idella, Pseudorasbora parva, Gambusia affinis, Rhodeus ocellatus and Puntius binotatus, in China [10,15-20]. In the present study, H. taichui metacercariae were detected in 15 fish species including 3 susceptible ones such as, H. leucisculus, C. carpio and T. houdemeri. Moreover, it was confirmed that 14 fish species, H. molitrix, H. maculatus, T. houdemeri, P. dispar, O. bidens, S. argentatus, A. rivularis, P. semifasciolatus, H. leucisculus, C. recurviceps, S. dabryi, M. lineata and C. dabryi, are recorded as new second intermediate hosts of H. taichui in the literature. On the other hand, it had been known that H. taichui is distributed in only Taiwan, China. However, H. taichui adults were collected from residents of GZAR, China after praziquantel treatment and magnesium salt purgation by the work of "Korea-China Collaborative Project of Control Strategies for Helminthiasis" [11].
Distribution of H. pumilio has been recorded in Guangdong and Fujian Provinces and Taiwan, China [9]. However, it has been confirmed by this study that H. pumilio is distributed in GZAR also. Seventeen fish species except P. parva, i.e., C. auratus, A. tonkinensis, H. maculates, H. molitrix, H. leucisculus, C. idella, T. houdemeri, M. fukiensis, P. dispar, O. bidens, S. argentatus, M. lineata, C. carpio, P. semifasciolatus, S. dabryi, C. recurviceps and C. dabryi are listed as the new second intermediate hosts of this fluke in China. On the other hand, it has been reported that the prevalence of H. pumilio is 0.5% in Zhangzhou of Fujian Province by the special processing way of fish dish [10]. Many human cases by this fluke may be present in GZAR also because of many residents like to eat raw fish and they can easily infect with FBT.
C. formosanus has been reported in Guangdong, Fujian, GZAR, and Taiwan, and 8 fish species, Anabas testudineus, Channa formosana, Clarias fuscus, Macropodus opercularis, G. affinis, C. autatus, C. carpio, C. idella, have been recorded as the second intermediate hosts of this fluke in China [10]. In the present study, 10 fish species including susceptible M. fukiensis were revealed to be the second intermediate host or the source of infection of C. formosanus. Among them, 9 fish species, M. fukiensis, A. tonkinensis, S. argentatus, H. molitrix, A. rivularis, H. leucisculus, M. lineate, S. dabryi and P. parva, were added as new second intermediate hosts for C. formosanus in China. Recently, metacercariae of this fluke were detected in some fish species, i.e., Esomus longimanus, P. brevis, C. repasson, O. hasseltii, and C. molitorella, from Lao PDR [15,20,21].
In China, 2 Metagonimus species, M. yokogawai and M. takahashii, have been reported. M. yokogawai has been distributed in Taiwan, Guangdong, Anhui, Hubei and Zhejiang, while M. takahashii has been reported in Anhui Province only. Twelve fish species, Abramis brama, Abramis ballerus (= Ballerus ballerus), Aspius aspius, Blicca bjoerkna, Carassius carassius, Chondrostoma nasus, Hemibarbus labeo, Leuciscus idus, Pelecus cultratus, Pseudobagrus fulvidraco (= Pelteobagrus fulvidraco), T. hakonensis and Zacco platypus, have been recorded as the second intermediate hosts of M. yokogawai in China [9]. In the present study, M. yokogawai metacercariae were detected in 18 fish species from Yangshou county, and only one fish species, Hemibarbus maculatus, from a market in Nanning, GZAR. Among them,16 fish species, Acrossocheilus hemispinus, Discogobio tetrabarbatus, H. maculates, Puntius semifasciolatus, Sinibrama macrops, Acheilognathus tonkinensis, Abbottina rivularis, Pseudogobio esocinus, C. auratus, Coreoperca whiteheadi, Opsariichthys bidens, Squalidus wolterstorffi, C. carpio, Ancherythroculter lini, Pseudohemiculter dispar and Hemiculter leucisculus, were newly recorded as the second intermediate host of M. yokogawai in China.
Morphologically, adults of Metagonimus sp. recovered from experimentally infected animals with metacercariae, which collected in fish from Yangshou county, were identical with those of M. yokogawai except the size of eggs. They have the larger ventral sucker, deviated to right side, than oral sucker, and the uterine loop passes through anterior border of both testes, whereas it courses between both testes in M. takahashii and M. miyatai. Their eggs, 25.4 × 15.6 µm in average size, were somewhat smaller than those of 3 Metagonimus species in Korea and Japan [22]. Biologically, the host specificity of this fluke relatively low when it is compared with those of 3 Metagonimus species, i.e. M. yokogawai, M. takahashii and M. miyatai, distributed in Korea [22]. As their fish intermediate hosts, Plecoglossus altivelis, Tribolodon hakonensis, T. taczanowskii and Lateolabrax japonicus for M. yokogawai, C. carpio and C. auratus for M. takahashii, Zacco platypus and Z. temmincki for M. miyatai have been reported in Korea [23,24].
C. sinensis infections are distributed in 22 out of 30 PRM (Province/Autonomous Region/Municipality) in China. In a nationwide survey, the prevalence was 0.4% among about 1.5 million people examined. Especially, the prevalence in Guangxi (1.39%), with those in Guangdong (2.09%), Anhui (1.37%) and Heilongjiang (1.19%), was much higher than those of the other regions. Based on data of nationwide survey, the number of clonorchiasis patients in China may be about 6 million [7-9]. On the other hand, as the second intermediate hosts of C. sinensis, 102 fish species in 59 genera 15 families have been reported in China including Taiwan [9]. However, metacercariae of C. sinensis were detected in only 3 fish species, H. maculatus, C. dabryi and H. leucisculus, in this study. Moreover, their infection rates and intensities were very low.
We thank Mr. Hongbo Xu and Miss Rui Lin, Division of Helminthiasis Prevention and Control, Guangxi Centre for Disease Prevention and Control, Nanning, China, for their help in our study, and Miss Jeong-A Kim and Soo-Jeong Park, Department of Parasitology, Gyeongsang National University School of Medicine, Jinju, Korea, for their help in examination of fish.
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Fig. 1
(A) Haplorchis taichui metacercaria detected in a freshwater fish, Hemiculter leucisculus, from a market of Nanning City. It is elliptical, has an oral sucker (OS), a baseball glove-shaped ventrogenital sac (arrow mark) with 11-18 rodlets and an O-shaped excretory bladder (EB). Scale bar = 50 µm. (B) Haplorchis pumilio metacercaria detected in a freshwater fish, Opsariichthys bidens, from Mashan-xian. It is elliptical, has an OS, a ventrogenital complex with 36-42 deer horn-like minute spines, and an O-shaped EB occupying large portion of posterior body. Scale bar = 50 µm.
kjp-47-249-g001.jpg
Fig. 2
(A) Centrocestus formosanus metacercaria detected in a freshwater fish, Microphysogobio fukiensis, from Mashan xian. It has 2 suckers, 32 circumoral spines around oral sucker (OS) arranged in 2 rows, and a X-shaped excretory bladder (EB) occupying greater portion of posterior body. Scale bar = 50 µm. (B) Metagonimus yokogawai metacercaria detected in a freshwater fish, Zacco platypus, from Yangshuo county. It is elliptical, has yellow brownish pigment granules scattering in body area of intestinal bifurcation, a ventral sucker (VS) deflectively located from median, and a V-shaped EB. Scale bar = 50 µm.
kjp-47-249-g002.jpg
Fig. 3
(A) Clonorchis sinensis metacercaria detected in a freshwater fish, Hemibarbus maculates, from Yangshuo county. It is elliptical, has nearly equal sized two suckers, brownish pigment granules scattering in the body, and an O-shaped excretory bladder occupying greater part of posterior body. Scale bar = 50 µm. (B) Echinochasmus perfoliatus metacercaria detected in a freshwater fish, Zacco platypus, from Yangshuo county. It is elliptical, has a transparent and double layered cyst wall, 24 dorsally interrupted collar spines (arrow marks), and a ventral sucker (VS) lying median on posterior 1/3 of body and as large as oral sucker (OS). Scale bar = 50 µm.
kjp-47-249-g003.jpg
Fig. 4
Metorchis taiwanensis metacercaria detected in a freshwater fish, Ctenopharyngodon idellus, from Binyang-xian. It is globular, has a double layered cyst wall (transparent and very thick outer layer and inner layer), nearly equal sized 2 suckers, and an O-shaped excretory bladder (EB). Scale bar = 50 µm.
kjp-47-249-g004.jpg
Fig. 5
Adults of Metagonimus yokogawai (A: unstained; B: Semichon's acetocarmine stained) were recovered from an experimental dog infected with metacercariae in fish from Yangshou county. They had a rightly deviated ventral sucker (VC), which is larger than the oral sucker (OS), muscular pharynx, moderately long esophagus and ceca, transversely long seminal vesicle (SV), round or elliptical ovary (O) and seminal receptacle (SR), and 2 obliquely adjacent testes (T). The uterine loop is passing through the anterior border of both testes. Scale bar = 200 µm.
kjp-47-249-g005.jpg
Table 1.
Freshwater fishes collected from 5 localities in Guangxi Zhuang Autonomous Region, China
Table 1.
Species of fish No. of fish examined in
Fusui Mashan Nanning Yangsuo Binyang Total
Hemibarbus maculatus - 4 11 10 - 25
Acheilognathus tonkinensis - 2 10 6 7 25
Zacoo platypus - - - 22 - 22
Carassius auratus - 2 11 4 4 21
Hypophthalmichthys molitrix 4 1 13 - - 18
Acrossocheilus hemispinus - - - 15 - 15
Discogobio tetrabarbatus - - - 14 - 14
Hemiculter leucisculus - - 3 1 10 14
Ctenopharyngodon idella 2 - - - 10 12
Pseudohemiculter dispar - 10 - 1 - 11
Opsariichythys bidens - 8 - 3 - 11
Puntius semifasciolatus - 4 - 7 - 11
Chanodichthys erythropterus 10 - - - - 10
Microphysogobio fukiensis - 10 - - - 10
Toxabramis houdemeri - - 10 - - 10
Abbottina rivularis - - 4 5 - 9
Cyprinus carpio 1 - 4 2 - 7
Squalidus argentatus - - 7 - - 7
Metzia lineata 2 2 - - 3 7
Cirrhinus molitorella 7 - - - - 7
Sinibrama macrops - - - 6 - 6
Pseudogobio esocinus - - - 5 - 5
Aristichthys nobilis 3 - - - - 3
Culter recurviceps 1 - 2 - - 3
Squalidus wolterstorffi - - - 2 - 2
Pseudorasbora parva 1 1 - - - 2
Saurogobio dabryi - - 2 - - 2
Chanodichthys dabryi - - 1 - 1 2
Ancherythroculter lini - - - 1 - 1
Oreochromis niloticus niloticus 7 1 3 - - 11
Coreoperca whiteheadi - - - 4 - 4
Total 38 45 81 108 35 307
Table 2.
Infection status of Haplorchis taichui metacercariae by the species of fish from a stream in Mashan-xian
Table 2.
Species of fish No. of fish examined No. (%) of fish infected No. of metacercariae detected
Total Range Average
Pseudohemiculter dispar 10 10 (100) 250 1-200 25.0
Opsariichthys bidens 8 8 (100) 224 4-82 28.0
Puntius semifasciolatus 4 - 9 - -
Carassius auratus 2 2 (100) 39 2-37 19.5
Metzia lineata 2 1 (50.0) 5 - 5.0
Hypophthalmichthys molitrix 1 1 (100) 13 - 13.0
Table 3.
Infection status of Haplorchis pumilio metacercariae by the species of fish from a stream in Mashan-xian
Table 3.
Species of fish No. of fish examined No. (%) of fish infected No. of metacercariae detected
Total Range Average
Microphysogobio fukiensis 10 6 (60.0) 58 1-22 9.7
Pseudohemiculter dispar 10 10 (100) 1,960 30-818 196.0
Opsariichthys bidens 8 8 (100) 3,328 150-1,096 416.0
Hemibarbus maculatus 4 4 (100) 151 25-45 37.8
Puntius semifasciolatus 4 - 886 - -
Carassius auratus 2 2 (100) 368 20-348 184.0
Metzia lineata 2 2 (100) 217 40-177 108.5
Hypophthalmichthys molitrix 1 1 (100) 85 - 85.0
Pseudorasbora parva 1 1 (100) 4 - 4.0
Table 4.
Infection status of Centrocestus formosanus metacercariae by the species of fish from a stream in Mashan-xian
Table 4.
Species of fish No. of fish examined No. (%) of fish infected No. of metacercariae detected
Total Range Average
Microphysogobio fukiensis 10 10 (100) 3,980 64-1,375 398.0
Metzia lineata 2 1 (50) 21 - 21.0
Pseudorasbora parva 1 1 (100) 1 - 1.0
Table 5.
Infection status of Haplorchis taichui metacercariae by the species of fish from a market in Nanning City
Table 5.
Species of fish No. of fish examined No. (%) of fish infected No. of metacercariae detected
Total Range Average
Hypophthalmichthys molitrix 13 13 (100) 691 7-159 53.2
Carassius auratus 11 11 (100) 306 4-120 27.8
Hemibarbus maculatus 11 10 (90.9) 401 6-92 40.1
Toxabramis houdemeri 10 10 (100) 1,930 1-485 193.0
Squalidus argentatus 7 3 (42.9) 45 5-20 15.0
Cyprinus carpio 4 3 (75.0) 589 1-356 196.3
Abbottina rivularis 4 2 (50.0) 14 2-12 7.0
Hemiculter leucisculus 3 3 (100) 716 105-396 238.7
Culter recurviceps 2 2 (100) 98 46-52 49.0
Saurogobio dabryi 2 2 (100) 130 35-95 65.0
Chanodichthys dabryi 1 1 (100) 55 - 55.0
Table 6.
Infection status of Haplorchis pumilio metacercariae by the species of fish from a market in Nanning City
Table 6.
Species of fish No. of fish examined No. (%) of fish infected No. of metacercariae detected
Total Range Average
Hypophthalmichthys molitrix 13 12 (92.3) 748 14-153 62.3
Carassius auratus 11 11 (100) 719 16-253 65.4
Hemibarbus maculatus 11 11 (100) 289 11-52 26.3
Acheilognathus tonkinensis 10 9 (90.0) 597 27-172 66.3
Toxabramis houdemeri 10 7 (70.0) 131 5-32 18.7
Squalidus argentatus 7 7 (100) 272 3-78 38.9
Cyprinus carpio 4 2 (75.0) 380 68-312 190.0
Hemiculter leucisculus 3 3 (100) 183 14-124 61.0
Saurogobio dabryi 2 2 (100) 188 88-100 94.0
Culter recurviceps 2 2 (100) 35 15-20 17.5
Chanodichthys dabryi 1 1 (100) 12 - 12.0
Table 7.
Infection status of Centrocestus formosanus metacercariae by the species of fish from a market in Nanning City
Table 7.
Species of fish No. of fish examined No. (%) of fish infected No. of metacercariae detected
Total Range Average
Acheilognathus tonkinensis 10 5 (50.0) 29 1-21 5.8
Squalidus argentatus 7 5 (71.4) 62 2-32 12.4
Cyprinus carpio 4 3 (75.0) 15 1-12 5.0
Hypophthalmichthys molitrix 4 3 (75.0) 17 2-13 5.7
Abbottina rivularis 4 4 (100) 56 7-22 14.0
Hemiculter leucisculus 3 1 (33.3) 55 - 55.0
Saurogobio dabryi 1 1 (100) 2 - 2.0
Table 8.
Infection status of Metagonimus yokogawai metacercariae by the species of fish collected from Yangshuo County
Table 8.
Species of fish No. of fish examined No. (%) of fish infected No. of metacercariae detected
Total Range Average
Zacco platypus 22 22 (100) 9,880 23-1,836 449.1
Acrossocheilus hemispinus 15 11 (73.3) 77 2-36 7.0
Discogobio tetrabarbatus 14 12 (85.7) 64 1-18 5.3
Hemibarbus maculatus 10 10 (100) 2,484 14-731 248.4
Puntius semifasciolatus 7 5 (71.4) 967 87-293 193.4
Sinibrama macrops 6 6 (100) 123 10-30 20.5
Acheilognathus tonkinensis 6 2 (33.3) 5 1-4 2.5
Abbottina rivularis 5 5 (100) 559 14-311 111.8
Pseudogobio esocinus 5 1 (20.0) 32 - 32.0
Carassius auratus 4 1 (25.0) 1 - 1.0
Coreoperca whiteheadi 4 1 (25.0) 2 - 2.0
Hemiculter sp. 4 3 (75.0) 224 5-209 74.7
Opsariichthys bidens 3 3 (100) 114 30-45 38.0
Squalidus wolterstorffi 2 2 (100) 31 3-28 15.5
Cyprinus carpio 2 1 (50.0) 13 - 13.0
Ancherythroculter lini 1 1 (100) 26 - 26.0
Pseudohemiculter dispar 1 1 (100) 31 - 31.0
Hemiculter leucisculus 1 1 (100) 34 - 34.0
Table 9.
Infection status of Haplorchis pumilio metacercariae by the species of fish from Binyang-xian
Table 9.
Species of fish No. of fish examined No. (%) of fish infected No. of metacercariae detected
Total Range Average
Hemiculter leucisculus 10 10 (100) 206 5-44 20.6
Ctenopharyngodon idella 10 10 (100) 712 22-144 71.2
Acheilognathus tonkinensis 7 7 (100) 732 68-150 104.6
Carassius auratus 4 4 (100) 334 42-125 83.5
Metzia lineata 3 3 (100) 62 17-23 20.7
Table 10.
Fish hosts infected with more than 100 metacercariae per fish by the trematode species
Table 10.
Species of flukes No. of fish host Fish hosts infected with more than 100 metacercariae/fish
Metagonimus yokogawai 18 Z. platypus, A. rivularis, H. maculatus, P. Semifasiolatus
Haplorchis taichui 15 H. leucisculus, C. carpio, T. houdemeri
Haplorchis pumilio 18 C. auratus, C. carpio, A. tonkinensis, O. bidens, M. lineata, P. dispar, P. Semifasiolatus
Centrocestus formosanus 10 M. fukiensis

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Fishborne Trematode Metacercariae in Freshwater Fish from Guangxi Zhuang Autonomous Region, China
Korean J Parasitol. 2009;47(3):249-257.   Published online August 28, 2009
DOI: https://doi.org/10.3347/kjp.2009.47.3.249
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Korean J Parasitol. 2009;47(3):249-257.   Published online August 28, 2009
DOI: https://doi.org/10.3347/kjp.2009.47.3.249
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Fishborne Trematode Metacercariae in Freshwater Fish from Guangxi Zhuang Autonomous Region, China
Image Image Image Image Image
Fig. 1 (A) Haplorchis taichui metacercaria detected in a freshwater fish, Hemiculter leucisculus, from a market of Nanning City. It is elliptical, has an oral sucker (OS), a baseball glove-shaped ventrogenital sac (arrow mark) with 11-18 rodlets and an O-shaped excretory bladder (EB). Scale bar = 50 µm. (B) Haplorchis pumilio metacercaria detected in a freshwater fish, Opsariichthys bidens, from Mashan-xian. It is elliptical, has an OS, a ventrogenital complex with 36-42 deer horn-like minute spines, and an O-shaped EB occupying large portion of posterior body. Scale bar = 50 µm.
Fig. 2 (A) Centrocestus formosanus metacercaria detected in a freshwater fish, Microphysogobio fukiensis, from Mashan xian. It has 2 suckers, 32 circumoral spines around oral sucker (OS) arranged in 2 rows, and a X-shaped excretory bladder (EB) occupying greater portion of posterior body. Scale bar = 50 µm. (B) Metagonimus yokogawai metacercaria detected in a freshwater fish, Zacco platypus, from Yangshuo county. It is elliptical, has yellow brownish pigment granules scattering in body area of intestinal bifurcation, a ventral sucker (VS) deflectively located from median, and a V-shaped EB. Scale bar = 50 µm.
Fig. 3 (A) Clonorchis sinensis metacercaria detected in a freshwater fish, Hemibarbus maculates, from Yangshuo county. It is elliptical, has nearly equal sized two suckers, brownish pigment granules scattering in the body, and an O-shaped excretory bladder occupying greater part of posterior body. Scale bar = 50 µm. (B) Echinochasmus perfoliatus metacercaria detected in a freshwater fish, Zacco platypus, from Yangshuo county. It is elliptical, has a transparent and double layered cyst wall, 24 dorsally interrupted collar spines (arrow marks), and a ventral sucker (VS) lying median on posterior 1/3 of body and as large as oral sucker (OS). Scale bar = 50 µm.
Fig. 4 Metorchis taiwanensis metacercaria detected in a freshwater fish, Ctenopharyngodon idellus, from Binyang-xian. It is globular, has a double layered cyst wall (transparent and very thick outer layer and inner layer), nearly equal sized 2 suckers, and an O-shaped excretory bladder (EB). Scale bar = 50 µm.
Fig. 5 Adults of Metagonimus yokogawai (A: unstained; B: Semichon's acetocarmine stained) were recovered from an experimental dog infected with metacercariae in fish from Yangshou county. They had a rightly deviated ventral sucker (VC), which is larger than the oral sucker (OS), muscular pharynx, moderately long esophagus and ceca, transversely long seminal vesicle (SV), round or elliptical ovary (O) and seminal receptacle (SR), and 2 obliquely adjacent testes (T). The uterine loop is passing through the anterior border of both testes. Scale bar = 200 µm.

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Fishborne Trematode Metacercariae in Freshwater Fish from Guangxi Zhuang Autonomous Region, China
Species of fish No. of fish examined in
Fusui Mashan Nanning Yangsuo Binyang Total Hemibarbus maculatus - 4 11 10 - 25 Acheilognathus tonkinensis - 2 10 6 7 25 Zacoo platypus - - - 22 - 22 Carassius auratus - 2 11 4 4 21 Hypophthalmichthys molitrix 4 1 13 - - 18 Acrossocheilus hemispinus - - - 15 - 15 Discogobio tetrabarbatus - - - 14 - 14 Hemiculter leucisculus - - 3 1 10 14 Ctenopharyngodon idella 2 - - - 10 12 Pseudohemiculter dispar - 10 - 1 - 11 Opsariichythys bidens - 8 - 3 - 11 Puntius semifasciolatus - 4 - 7 - 11 Chanodichthys erythropterus 10 - - - - 10 Microphysogobio fukiensis - 10 - - - 10 Toxabramis houdemeri - - 10 - - 10 Abbottina rivularis - - 4 5 - 9 Cyprinus carpio 1 - 4 2 - 7 Squalidus argentatus - - 7 - - 7 Metzia lineata 2 2 - - 3 7 Cirrhinus molitorella 7 - - - - 7 Sinibrama macrops - - - 6 - 6 Pseudogobio esocinus - - - 5 - 5 Aristichthys nobilis 3 - - - - 3 Culter recurviceps 1 - 2 - - 3 Squalidus wolterstorffi - - - 2 - 2 Pseudorasbora parva 1 1 - - - 2 Saurogobio dabryi - - 2 - - 2 Chanodichthys dabryi - - 1 - 1 2 Ancherythroculter lini - - - 1 - 1 Oreochromis niloticus niloticus 7 1 3 - - 11 Coreoperca whiteheadi - - - 4 - 4 Total 38 45 81 108 35 307 Species of fish No. of fish examined No. (%) of fish infected No. of metacercariae detected
Total Range Average Pseudohemiculter dispar 10 10 (100) 250 1-200 25.0 Opsariichthys bidens 8 8 (100) 224 4-82 28.0 Puntius semifasciolatus 4 - 9 - - Carassius auratus 2 2 (100) 39 2-37 19.5 Metzia lineata 2 1 (50.0) 5 - 5.0 Hypophthalmichthys molitrix 1 1 (100) 13 - 13.0 Species of fish No. of fish examined No. (%) of fish infected No. of metacercariae detected
Total Range Average Microphysogobio fukiensis 10 6 (60.0) 58 1-22 9.7 Pseudohemiculter dispar 10 10 (100) 1,960 30-818 196.0 Opsariichthys bidens 8 8 (100) 3,328 150-1,096 416.0 Hemibarbus maculatus 4 4 (100) 151 25-45 37.8 Puntius semifasciolatus 4 - 886 - - Carassius auratus 2 2 (100) 368 20-348 184.0 Metzia lineata 2 2 (100) 217 40-177 108.5 Hypophthalmichthys molitrix 1 1 (100) 85 - 85.0 Pseudorasbora parva 1 1 (100) 4 - 4.0 Species of fish No. of fish examined No. (%) of fish infected No. of metacercariae detected
Total Range Average Microphysogobio fukiensis 10 10 (100) 3,980 64-1,375 398.0 Metzia lineata 2 1 (50) 21 - 21.0 Pseudorasbora parva 1 1 (100) 1 - 1.0 Species of fish No. of fish examined No. (%) of fish infected No. of metacercariae detected
Total Range Average Hypophthalmichthys molitrix 13 13 (100) 691 7-159 53.2 Carassius auratus 11 11 (100) 306 4-120 27.8 Hemibarbus maculatus 11 10 (90.9) 401 6-92 40.1 Toxabramis houdemeri 10 10 (100) 1,930 1-485 193.0 Squalidus argentatus 7 3 (42.9) 45 5-20 15.0 Cyprinus carpio 4 3 (75.0) 589 1-356 196.3 Abbottina rivularis 4 2 (50.0) 14 2-12 7.0 Hemiculter leucisculus 3 3 (100) 716 105-396 238.7 Culter recurviceps 2 2 (100) 98 46-52 49.0 Saurogobio dabryi 2 2 (100) 130 35-95 65.0 Chanodichthys dabryi 1 1 (100) 55 - 55.0 Species of fish No. of fish examined No. (%) of fish infected No. of metacercariae detected
Total Range Average Hypophthalmichthys molitrix 13 12 (92.3) 748 14-153 62.3 Carassius auratus 11 11 (100) 719 16-253 65.4 Hemibarbus maculatus 11 11 (100) 289 11-52 26.3 Acheilognathus tonkinensis 10 9 (90.0) 597 27-172 66.3 Toxabramis houdemeri 10 7 (70.0) 131 5-32 18.7 Squalidus argentatus 7 7 (100) 272 3-78 38.9 Cyprinus carpio 4 2 (75.0) 380 68-312 190.0 Hemiculter leucisculus 3 3 (100) 183 14-124 61.0 Saurogobio dabryi 2 2 (100) 188 88-100 94.0 Culter recurviceps 2 2 (100) 35 15-20 17.5 Chanodichthys dabryi 1 1 (100) 12 - 12.0 Species of fish No. of fish examined No. (%) of fish infected No. of metacercariae detected
Total Range Average Acheilognathus tonkinensis 10 5 (50.0) 29 1-21 5.8 Squalidus argentatus 7 5 (71.4) 62 2-32 12.4 Cyprinus carpio 4 3 (75.0) 15 1-12 5.0 Hypophthalmichthys molitrix 4 3 (75.0) 17 2-13 5.7 Abbottina rivularis 4 4 (100) 56 7-22 14.0 Hemiculter leucisculus 3 1 (33.3) 55 - 55.0 Saurogobio dabryi 1 1 (100) 2 - 2.0 Species of fish No. of fish examined No. (%) of fish infected No. of metacercariae detected
Total Range Average Zacco platypus 22 22 (100) 9,880 23-1,836 449.1 Acrossocheilus hemispinus 15 11 (73.3) 77 2-36 7.0 Discogobio tetrabarbatus 14 12 (85.7) 64 1-18 5.3 Hemibarbus maculatus 10 10 (100) 2,484 14-731 248.4 Puntius semifasciolatus 7 5 (71.4) 967 87-293 193.4 Sinibrama macrops 6 6 (100) 123 10-30 20.5 Acheilognathus tonkinensis 6 2 (33.3) 5 1-4 2.5 Abbottina rivularis 5 5 (100) 559 14-311 111.8 Pseudogobio esocinus 5 1 (20.0) 32 - 32.0 Carassius auratus 4 1 (25.0) 1 - 1.0 Coreoperca whiteheadi 4 1 (25.0) 2 - 2.0 Hemiculter sp. 4 3 (75.0) 224 5-209 74.7 Opsariichthys bidens 3 3 (100) 114 30-45 38.0 Squalidus wolterstorffi 2 2 (100) 31 3-28 15.5 Cyprinus carpio 2 1 (50.0) 13 - 13.0 Ancherythroculter lini 1 1 (100) 26 - 26.0 Pseudohemiculter dispar 1 1 (100) 31 - 31.0 Hemiculter leucisculus 1 1 (100) 34 - 34.0 Species of fish No. of fish examined No. (%) of fish infected No. of metacercariae detected
Total Range Average Hemiculter leucisculus 10 10 (100) 206 5-44 20.6 Ctenopharyngodon idella 10 10 (100) 712 22-144 71.2 Acheilognathus tonkinensis 7 7 (100) 732 68-150 104.6 Carassius auratus 4 4 (100) 334 42-125 83.5 Metzia lineata 3 3 (100) 62 17-23 20.7 Species of flukes No. of fish host Fish hosts infected with more than 100 metacercariae/fish Metagonimus yokogawai 18 Z. platypus, A. rivularis, H. maculatus, P. Semifasiolatus Haplorchis taichui 15 H. leucisculus, C. carpio, T. houdemeri Haplorchis pumilio 18 C. auratus, C. carpio, A. tonkinensis, O. bidens, M. lineata, P. dispar, P. Semifasiolatus Centrocestus formosanus 10 M. fukiensis
Table 1. Freshwater fishes collected from 5 localities in Guangxi Zhuang Autonomous Region, China
Table 2. Infection status of Haplorchis taichui metacercariae by the species of fish from a stream in Mashan-xian
Table 3. Infection status of Haplorchis pumilio metacercariae by the species of fish from a stream in Mashan-xian
Table 4. Infection status of Centrocestus formosanus metacercariae by the species of fish from a stream in Mashan-xian
Table 5. Infection status of Haplorchis taichui metacercariae by the species of fish from a market in Nanning City
Table 6. Infection status of Haplorchis pumilio metacercariae by the species of fish from a market in Nanning City
Table 7. Infection status of Centrocestus formosanus metacercariae by the species of fish from a market in Nanning City
Table 8. Infection status of Metagonimus yokogawai metacercariae by the species of fish collected from Yangshuo County
Table 9. Infection status of Haplorchis pumilio metacercariae by the species of fish from Binyang-xian
Table 10. Fish hosts infected with more than 100 metacercariae per fish by the trematode species

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PHD : Parasites, Hosts and Diseases

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