Abstract
Isthmiophora hortensis (Digenea: Echinostomatidae) is a dominant echinostome in animal reservoir hosts and humans in the Republic of Korea (Korea). We intended to investigate the infection status with this echinostome species in the several species of wild animals and describe the morphological characteristics in the faunistic view point. A total of 175 animal carcasses belonging to 3 families, i.e., Canidae, Felidae and Mustelidae, were collected from the southern regions of Korea from March 2010 to July 2017. Isthmiophora spp. worms were recovered from the small intestines of each animal under a stereomicroscope after washing of intestinal contents. Isthmiophora hortensis was recovered from 4 species of wild carnivores, i.e., Nyctereutes procyonoides (3/107: 2.8%), Mustela sibirica (11/31: 35.5%), Meles lucurus (2/3: 33.3%) and Martes flavigula (1/2: 50%). The other 3 carnivores comprising stray dogs, cat and leopard cat were negative for I. hortensis infection (0/2, 0/10 and 0/12, respectively). Specimens obtained from the Lutra lutra (6/8: 75%) were identified as a distinct species, I. inermis, by morphological comparison. Isthmiophora inermis has thinner body, elongate testes and different anterior limits of vitelline fields. Detailed morphological descriptions and comparisons with the morphological characteristics are provided. Conclusively, it was confirmed for the first time that 3 species of mustelid mammals, i.e., M. sibirica, M. lucurus, and M. flavigula, are to be the new definitive hosts of I. hortensis in Korea. Additionally, I. inermis is to be newly added in the Korean echinostome fauna.
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Key words: Isthmiophora hortensis, Isthmiophora inermis, mustelidae, wild carnivore
INTRODUCTION
Isthmiophora hortensis (Asada, 1926) (Digenea: Echinostomatidae) is an echinostome trematode species characterized by the possession a collar with 27 spines and has medical and veterinary importance. Human infection with
I. hortensis has been reported frequently in East Asian countries such as China, Japan and the Republic of Korea (=Korea) [
1].
Due to its public health importance, the life cycle of the species has been studied extensively. Freshwater snails of the family Lymnaeidae Rafinesque, 1815 are known to serve as first intermediate hosts [
2–
4], while freshwater fishes and frogs have been reported as second intermediate hosts [
3,
5–
10]. Additionally, a wide range of small mammals are known as respective definitive hosts, such as the rat (reported in Japan by Asada, 1926) [
21], black-striped field mouse
Apodemus agrarius (Pallas), Manchurian reed vole
Microtus fortis pelliceus Thomas, domestic mouse
Mus musculus L., brown rat
Rattus norvegicus (Berkenhout), black rat
R. rattus L., Daurian pika
Ochotona dauurica (Pallas), domestc dog
Canis lupus familiaris L., domestic cat
Felis catus L., Japanese weasel
Mustela itatsi Temminck (=
Lutreola itatsi itatsi) and raccoon
Procyon lotor L. [
12–
25]. Recently, Sohn et al. reported two additional species, namely, the raccoon dog
Nyctereutes procyonoides (Gray) and wild boar
Sus scrofa L., to the list of known definitive hosts of
I. hortensis [
23].
Ishtmiophora inermis (Fuhrmann, 1904) is one of 6 species belonging to the genus
Isthmiophora. This species is morphologically very similar to
I. hortensis, but has thinner body, elongate testes and different anterior limits of vitelline fields [
26]. Moreover, this species has a somewhat different host range than
I. hortensis. Unlike the hosts of
I. hortensis as we mentioned above, this species has been found mainly in otters i.e.,
Lutra sp.,
L. lutra and
Lontra canadensis (Schreber, 1777) [
18,
27–
32]. Eurasian otter has been found in Korea as well, but the distribution of
I. inermis is still unknown until present study.
Considering the life cycle of Isthmiophora flukes and their known hosts, wild mammals and especially carnivorous or omnivorous animals such as mustelids seem to be suitable hosts for I. hortensis. However, their infection status in Korea is not well known. Therefore, the present study aimed to investigate the infection status of I. hortensis for wild mammals in Korea and to determine the range of its definitive hosts. The present study provides reports on yellow-throated marten Martes flavigula (Boddaert), Aisan badger Meles lucurus (Hodgson) and Siberian weasel M. sibirica Pallas as new host records of I. hortensis, and presents a detailed overview of its infection status in Korea. In addition, we include detailed morphological characteristics of I. inermis, found from the intestines of Eurasian otter Lutra lutra, as a new member of the Korean parasite fauna.
MATERIALS AND METHODS
Collecting specimens
Carcasses of wild carnivores were collected from March 2010 to July 2017. A total of 175 wild carnivores belonging to three families comprising Canidae, Felidae and Mustelidae were collected and examined. Collection, identification and necropsy of the host animals were conducted with the support of several wild animal rescue centers or wildlife related institutes, namely, the Wildlife Center of Chungbuk (WCC), Cheongju-si, Chungcheongbuk-do, Korea, the Chungnam Wild Animal Rescue Center (CNWARC), Yesan-gun, Chungcheongnam-do, Korea, the Korean National Park Service Species Restoration Technology Institute (KNPSSRTI), Gurye-gun, Jeollanam-do, Korea and the Conservation Genome Resource Bank for Korean Wildlife (CGRB), Seoul, Korea, as well as small-scale college laboratories. All of the examined hosts were collected from the Korean peninsula.
Examined hosts included stray dogs C. lupus familiaris L. (n=2), Korean raccoon dog N. procyonoides koreensis (Gray) (n=107), stray cats F. cactus L. (n=10), Amur leopard cats Prionailurus bengalensis euptilurus (Elliot) (n=12), Siberian weasels M. sibirica (n=31), Eurasian otters L. lutra L. (n=8), Asian badgers M. lucurus (n=3) and yellow-throated martens M. flavigula (n=2). Most of the animals were dead during rescue/care in the wildlife rescue center, or found on the road as a carcass.
The visceral organs were extracted from each dead body, and the lumen was exposed by a longitudinal incision.
Isthmiophora spp. were recovered from the visceral organs using the filtration method [
36]. Parasite numbers were then recorded and recovered specimens were stored in fixative agents (70% ethanol or 10% neutral buffered formalin) for further research. Detailed information concerning infection status and locality of positive cases is provided in
Table 1.
Identification of species was based on the key to the species of
Isthmiophora provided by Kostadinova and Gibson [
26]. Two species,
I. hortensis and
I. intermis, were distinguished using morphological observations. Based on the morphological condition of specimens and the representativeness among the morphological differences, 12
I. hortensis and 12
I. inermis were chosen for morphological observation. Specimens of
I. hortensis (host code no. B417) was obtained from a
M. sibirica collected from Cheongju (city) in 2011 and
I. inermis (host code no. B1330) was obtained from a
L. lutra collected from Cheongju in 2015. They were stained with Semichon’s acetocarmine and observed under light microscopy on a mounted slide in Permount (Fisher Scientific) [
33]. The voucher specimens were deposited at the National Institute of Biological Resources (NIBR), Incheon Metropolitan City, Korea and the Parasite Resource Bank (PRB), Cheongju-si, Chungcheongbuk-do, Korea.
Abbreviations used in the present study are as follows: BL: body length; BW: maximum body width; CL: collar length; CW: collar width; NCS: number of collar spines; OSL: oral sucker length; OSW: oral sucker width; PL: prepharynx length; PHL: pharynx length; PHW: pharynx width; ESL: esophagus length; CSL: cirrus sac length; CSW: cirrus sac width; SVL: seminal vesicle length; SVW: seminal vesicle width; VSL: ventral sucker length; VSW: ventral sucker width; OVL: ovary length; OVW: ovary width; MEL: Mehlis’ gland length; MEW: Mehlis’ gland width; ATL: anterior testis length; ATW: anterior testis width; PTL: posterior testis length; PTW: posterior testis width; EL: egg length; EW: egg width; FO: forebody length (distance from the anterior end to the anterior margin of the ventral sucker); U: uterine field length (distance from the anterior margin of the ovary to the posterior margin of the ventral sucker); and T: post-testicular field length. The size and proportions of standard structures relative to body length were calculated as described by Kostadinova [
34]. Measurements are shown in
Table 2.
RESULTS
Among the 175 hosts examined, 23 animals were positive for
Isthmiophora flukes (13%).
Isthmiophora flukes were found in all mustelid hosts and included Siberian weasel (11/31, 35.5%), Asian badger (2/3, 33.3%), Eurasian otter (6/8, 75%) and yellow-throated marten (1/2, 50%). Furthermore, only 3 of the 107 raccoon dogs (2.8%) were infected with
Isthmiophora flukes. Dogs, cats, and leopard cats were negative for these flukes. However, the flukes that were found in these animals are thought to be
I. hortensis. Moreover, morphological examination revealed that all the
Isthmiophora flukes found in Eurasian otters were
I. inermis. Detailed information concerning infection status and locality of positive cases is provided in
Table 1.
Host: Martes flavigula, Meles lucurus, Mustela sibirica, Nyctereutes procyonoides
Localities: Chungcheongbuk-do (Cheongju-si), Chungcheong-nam-do (Boryeong-si, Cheongyang-gun, Hongseong-gun, Sejong-si, Taean-gun and Yesan-gun) and Ulsan (Ulju-gun); Republic of Korea.
Description (
Fig. 1, n=12): Body thin, foliated, dorso-ventrally flattened. Maximum body width at the level of ovary. Forebody short to long (FO/BL=12–19%). Tegumental spine present, densely distributed in forebody but less dense in hind body. Collar reniform, small. Ventral lappets poorly developed. Collar spines 27 in number, angle spines aligned in double row (2 ventral and 2 dorsal), lateral spines in single row, and dorsal spines in double row. Oral sucker subterminal, subspherical, muscular. Prepharynx present. Pharynx muscular, elongate-oval. Oesophagus short. Intestinal bifurcation in front of ventral sucker. Caeca blind, narrow, overlapped by vitelline follicles, almost reaching posterior end. Ventral sucker subspherical, well-developed, muscular.
Testes 2, tandem, large, oval to irregular shaped, located in equatorial region of body. Post testicular region long (T/BL=36–47%). Cirrus sac oval, muscular, located antero-dorsal to ventral sucker, included elongated seminal vesicle with curved pars prostatica. Cirrus tubular, armed with spines. Genital pore located posterior to intestinal bifurcation.
Ovary spherical to oval, dextral to median, close to ventral sucker (U/BL=5–15%). Mehlis’ gland large, sub-median, contiguous but slightly behind ovary. Uterus intercaecal, short. Eggs oval, yellowish. Vitelline follicles small, distributed from the level of ovary to posterior extremity, occupy each side of the body and overlapped at post testicular field. Excretory vesicle Y-shaped.
Isthmiophora inermis (Fuhrmann, 1904) Kostadinova and Gibson, 2002
Host: Lutra lutra
Localities: Chungcheongbuk-do (Cheongju-si and Chungju-si), Chungcheongnam-do (Yesan-gun), and Jeollanam-do (Gurye-gun); Republic of Korea
Descriptions (Fig. 2, n=12): Body thin, elongated and cylindrical (BW/BL=10–12%). Maximum body width at level of anterior testis or ventral sucker. Forebody short (FO/BL=11–17%). Tegumental spine obscure.
Collar weakly developed, armed with 27 spines. Ventral lappets poorly developed. Oral sucker subterminal, subspherical, muscular. Prepharynx present. Pharynx muscular, elongate-oval. Oesophagus relatively short, bifurcated slightly at anterior region of the ventral sucker. Ventral sucker large, subspherical, muscular, well-developed.
Testes 2, tandem, elongated, oval shaped. Post testicular region very long (47–55%). Cirrus sac located between intestinal bifurcation and ventral sucker, oval, muscular, includes elongated, curved seminal vesicle with convoluted and long pars prostatica. Cirrus tubular. Genital pore located posterior to intestinal bifurcation.
Ovary spherical, entire, dextral, located somewhat in spaces anterior to anterior testis. Mehlis’ gland well-developed, median. Uterus short (U/BL=6–10%), filled with eggs. Metraterm muscular. Vitelline follicles well-developed, covering region starting from posterior end to near anterior border of anterior testis.
DISCUSSION
Morphological observations of stained slide specimens representing the two groups of
Isthmiophora flukes indicated that the characteristics of specimens matched well with the diagnostic characteristics of the genus
Isthmiophora [
26,
34]. All specimens had 27 collar spines and exhibited the characteristics regarded as the major attributes of the genus
Isthmiophora as noted by Kostadinova and Gibson [
26]. Observations revealed a slightly greater anterior position of the testes (T/BL=36–55%), armed cirrus, small head collar with not well-developed ventral lappets, longer oral spines than aboral, short forebody (FO/BL=11–17%) and uterus (U/BL=5–14%), and large eggs.
According to the differential keys of
Isthmiophora suggested by Kostadinova and Gibson [
26], our specimens were identified as comprising two
Isthmiophora species,
I. hortensis and
I. inermis. All specimens collected from animal hosts investigated in this study, with the exception of Eurasian otters, had morphological characteristics identical to those of
I. hortensis, which was the only species reported previously in Korea.
I. hortensis is regarded as very similar morphologically to
I. melis, and the only difference between the two species is the position of cirrus sac (located between intestinal bifurcation and ventral sucker or antero-dorsal to the ventral sucker). Recently, Sohn et al. investigated body indices of
I. hortensis obtained from 4 species of terrestrial mammals, namely,
A. agrarius, F. cactus, N. procyonoides and
S. scrofa, and compared results with those of experimentally infected albino rats (metacercariae were obtained from the Korean dark sleeper,
Odontobutis platycephala Iwata & Jeon) in Korea [
23]. They also noted that
I. hortensis has a high similarity with
I. melis and that it is very difficult to distinguish the two species, which can only be accomplished using a morphological aspect such as body indices. Our results also indicate that body indices are very similar to those of
I. melis; however, our observations indicate that the position of the cirrus sac is similar to that reported by Kostadinova and Gibson [
26].
I. inermis can be distinguishable from
I. hortensis by its slender body, rather elongated testes and anterior limits of the vitelline fields at the level of the anterior testis [
26]. These features can also be checked in our specimens collected from
L. lutra. Additionally, morphometric comparisons supported the species identifications (
Table 2). Observations showed that specimens of both species did not differ much since measurements of size overlapped for most body parts. However, the measurements support the distinction of species based on differences in the ratios of body parts. In comparison with
I. hortensis,
I. inermis had a slender body, BW/BL: 9–12% (11%) and longer post-testicular fields, T/BL: 47–55% (50%). The BW and T ratio relative to the BL of
I. hortensis were 11–19% (15%) and 36–47% (41%), respectively (
Table 2).
The specimens collected from
Lutra lutra were all identified as
I. inermis, which had never been reported before as a member of the Korean parasite fauna.
Isthmiophora inermis was primarily described as
Euparyphium inerme in a Lutra sp. from Java, Indonesia [
27], but Kostadinova and Gibson [
26] considered this species as a member of the genus
Isthmiophora and transferred it from the genus
Euparyphium to
Isthmiophora. As in the present study,
I. inermis has been mainly detected from otters (
Lutra sp., and
L. lutra) in Eurasian countries such as China, Indonesia (Java), the Russian Far East and Vietnam [
18,
27–
31]. Additionally, several suspicious findings of this species were recorded from North America [
32]. The only known case of a non-mustelid host involved dogs in India [
35]. Our results suggest that the species could be found along with the distribution of its main host
L. lutra, and Korea is a new location for its distribution.
The generic conception of the genus
Isthmiophora as re-defined by Kostadinova and Gibson [
26] provides insights into the life history and host range of species identified in this study by comparison with other members of the genus. Generally, they have been known to use mammals as definitive hosts [
26,
34]. Among the known host species, mustelids represent a large portion of their host diversity. With the exception of two species having 29 collar spines,
I. lukjanovi Chertkova, 1971 [
36] and
I. citellicola Kadenatsii in Skrjabin & Bashkirova, 1956 [
37], which were only reported from
Gazella subgutturosa and
Citellus pygmaeus, the other 4 species are known to use at least one species of mustelid. The type species
I. melis was reported from over 10 species of mustelids [
29], and otters are known to act as definitive hosts of
I. inermis [
27–
32]. A North American species,
I. beaveri, was reported from a mustelid host,
Neovison vison (Schreber) (=
Mustela vison), and also from experimentally infected ferrets [
26,
38,
39]. Several authors have noted the importance of mustelids as hosts of
Isthmiophora flukes [
13,
40,
41].
Isthmiophora hortensis has been known to use mammals as its definitive host. It is our understanding that the host list includes 11 animals belong to 6 families as follows: Canidae (
Canis lupus and
N. procyonoides), Felidae (
F. catus), Ochotonidae (
Ochotona dauurica), Muridae (
A. agrarius, R. norvegicus, R. rattus, fortisM. pellceus, M. musculus), Mustelidae (
M. itatsi), Procyonidae (
P. lotor) and Suidae (
S. scrofa) in Korea, China, Japan, Vietnam and the Russian Far East [
12,
14–
25,
29]. However, only one species of mustelid, the Japanese weasel
M. itatsi, has been reported as a host of
I. hortensis [
13].
As with other
Isthmiophora species that have 27 collar spines,
I. hortensis was also found to use mustelids as its definitive hosts. In the present study, we found
I. hortensis from 3 species of mustelids, i. e.,
M. sibirica, M. lucurus and
M. flavigula. Furthermore, their infection rates seem relatively higher than those for other host species reported previously in Korea. Seo et al. [
14] examined a total of 624 rodents comprising 5 species (
A. agrarius, R. norvegicus, R. rattus, M. musculus and
M. fortis) and a species of shrew,
Crocidura lasiura Dobson (=
C. russula) from the northern region of the Republic of Korea. They found
I. hortensis from 15 rodents and the maximum number of infections was 134 from
R. rattus. An additional survey was conducted inside a campus located in Seoul by Seo et al. [
15]. They found only 4 positive rats among 325 rats (
R. norvegicus). Follow-up studies of rodent species were then conducted by several authors, but the infection rates were not very high and measured 16/170 (rats) by Seo et al. [
16], 1/34 (
R. rattus) by Ahn and Ryang [
42], and 6/236 (
A. agrarius) by Sohn et al. [
23]. The number of infections from the 3 studies was estimated as 1 to 65. Cho et al. [
17] found
I. hortensis from another host (dog) with an infection rate of 3.9% (4/102). Analysis of cats showed similar results.
Two surveys were conducted for helminth parasites of stray cats in Korea.
I. hortensis was found in 5 of 438 (1.1%) cats in Busan, and 6 of 400 (1.5%) cats near 5 major river basins. The numbers of infection were 1–485 and 1–59, respectively [
21,
25]. Although the number of animals examined in the present study was not large, the infection rate and number of infections in mustelid hosts were relatively high (
Table 1). On the other hand, our investigation of the infection status of the raccoon dog revealed results similar to those of a previously reported case of a dog (2.8 vs. 3.9%, respectively) and a smaller infection number (1–5 vs. 2–32). These results indicate that mustelid hosts act as predominant hosts of
I. hortensis in wild carnivores within Korea.
The existence of additional species of
Isthmiophora in Korea may prompt a revision of previously believed information on
I. hortensis. The classical identifications of echinostome metacercariae depend only on the number of collar spines [
9]. This resulted in little impetus previously to consider distinguishing 2
Isthmiophora species that had the same number of collar spines (27–28) using the classical morphological identification. If fishes can mediate the metacercariae of
I. inermis, then previously reported data may include the misidentification of
I. inermis. Indeed, a consideration of the habitat and eating habits of
L. lutra suggests strongly that freshwater fishes are the main intermediate host of
I. inermis rather than other intermediate hosts.
Lutra lutra has been known to use freshwater fishes as its main prey. Furthermore, Choe et al. [
43,
44] recorded cases of fluke species in Korea,
Pegosomum bubulcum [
43] and
Chaunocephalus ferox [
44], which had 27 collar spines and were thought to use freshwater fishes as intermediate hosts. Recently, Sohn and Na [
45] found unidentified echinostomatid metacercariae that are morphologically very similar with those of
I. hortensis metacercariae from freshwater fishes caught from Junam-jeosuji (reservoir) and Woopo-neup (swamp) in Gyeongsangnam-do, Korea. In this situation, clarification of the intermediate host of
I. inermis is considered essential before metacercariae investigation. In addition, certainty is needed regarding differential diagnosis between metacercariae that have 27 collar spines, and such investigations should involve molecular analysis. Human infections of
I. inermis are also an issue that can’t be overlooked, and their potential for human infection needs to be investigated.
In conclusion, the results of the present study revealed the infection status of I. hortensis in various wild mammals and the existence of an additional Isthmiophora species, I. inermis, in Eurasian otters, in Korea. We provided their detailed morphometric comparisons, and showed the morphological differences between two species. However, our study is limited that the identification is based only morphological observations. DNA analysis should be conducted in near future for better understanding about the differences between Isthmiophora species and also the taxonomic aspects. As with other Isthmiophora species that have 27 collar spines, Isthmiophora hortensis appeared to have a significant relationship with mustelid hosts, and we added three more species to the host list of Isthmiophora hortensis. We also showed the relatively high prevalence of I. hortensis infection in mustelid hosts. Considering the present results and ecology of mustelid hosts, they seem to play an important role as dominant hosts in the life cycle of I. hortensis in the Korean ecosystem.
Notes
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CONFLICT OF INTEREST
The authors declare that they have no conflict of interest with this article.
ACKNOWLEDGMENTS
The authors are grateful to Dr. Youngsun Lee (Gyeonggi Northern Livestock and Veterinary Service, Yangju, Korea) and Mr. Joon Seok Lee (Chungnam Wild Animal Rescue Center, Yesan, Korea), for their assistance with sample collections. This work was supported by a grant from the National Institute of Biological Resources (NIBR), which is funded by the Ministry of Environment (MOE) of the Republic of Korea (NIBR no. 2015-02-001) and the Parasite Resource Bank of Korea of the National Research Resource Center (2012-0000037) of the Republic of Korea.
Fig. 1Descriptions of Isthmiophora hortensis (Asada, 1926) recovered from a Siberian weasel Mustela sibirica Pallas. (A) Entire worm, (B) Head collar. (C) Terminal genitalia, (D) Body part showing the anterior distribution of vitelline follicles (black arrowhead) Scale bars: (A) 2 mm. (B–C) 200 μm. (D) 500 μm.
Fig. 2Descriptions of Isthmiophora inermis (Fuhrmann, 1904) recovered from a Eurasian otter Lutra lutra L. (A) Entire worm, (B) Head collar. (C) Terminal genitalia, (D) Body part showing the anterior distribution of vitelline follicles (black arrowhead) Scale bars: (A) 2 mm. (B, C) 200 μm. (D) 500 μm.
Table 1Prevalence of Isthmiophora spp. in wild mammals from the Republic of Korea
Table 1
|
Host species |
No. of animals examined |
No. (%) of animals positive |
No. of worms recovered |
Survey areas†
|
|
Canidae |
|
|
|
|
|
Canis lupus familiaris (stray dog) |
22 |
0 (0) |
- |
- |
|
Nyctereutes procyonoides koreensis
|
107 |
3 (2.8) |
1–5 (3±2) |
Cheongju (3/107) |
|
Felidae |
|
Felis cactus (stray cat) |
10 |
0 (0) |
- |
- |
|
Prionailurus bengalensis euptilurus
|
12 |
0 (0) |
- |
- |
|
|
Mustelidae |
|
Mustela sibirica
|
31 |
11 (35.5) |
2–150 (54±56) |
Cheongju (7/10), Taean (1/1), Hongseong (1/2), Cheongyang (2/2), Sejong (1/1) |
|
Meles lucurus
|
3 |
2 (33.3) |
20–24 (22±3) |
Ulju (1/1), Yesan (1/1) |
|
Martes flavigula
|
2 |
1 (50) |
5 |
Boryeong (1/1) |
|
|
Lutra lutra
|
8 |
6 (75) |
98–410 (268±134) |
Yesan (1/1), Cheongju (2/2), Gurye (1/1), Chungju (1/1) |
Table 2Morphometric comparisons of Isthmiophora hortensis (Asada, 1926) and I. inermis (Fuhrmann, 1904) in the present study
Table 2
|
Species |
I. hortensis (Asada, 1926) |
I. inermis (Fuhrmann, 1904) |
|
|
|
|
Hosts |
Mustela sibirica Pallas (n=12) |
Lutra lutra L. (n=12) |
|
|
|
|
Min. |
Max. |
Average |
Min. |
Max. |
Average |
|
BL |
5,707 |
8,585 |
6,913 |
6,273 |
9,446 |
7,360 |
|
|
BW |
861 |
1,107 |
961 |
615 |
984 |
820 |
|
|
CL |
206 |
265 |
231 |
216 |
372 |
273 |
|
|
CW |
343 |
412 |
372 |
304 |
451 |
392 |
|
|
DSpL |
42 |
57 |
52 |
66 |
83 |
74 |
|
|
DSpW |
9 |
14 |
12 |
14 |
20 |
16 |
|
|
LSpL |
46 |
56 |
52 |
47 |
70 |
58 |
|
|
LSpW |
7 |
14 |
10 |
8 |
16 |
12 |
|
|
ASpL |
50 |
64 |
57 |
66 |
83 |
73 |
|
|
ASpW |
14 |
17 |
14 |
19 |
15 |
17 |
|
|
OSL |
167 |
216 |
189 |
137 |
216 |
180 |
|
|
OSW |
186 |
274 |
219 |
147 |
245 |
205 |
|
|
PL |
20 |
88 |
46 |
0 |
88 |
49 |
|
|
PHL |
167 |
206 |
180 |
108 |
186 |
159 |
|
|
PHW |
142 |
201 |
172 |
118 |
186 |
150 |
|
|
OL |
235 |
451 |
315 |
294 |
588 |
452 |
|
|
CSL |
294 |
608 |
444 |
333 |
539 |
453 |
|
|
CSW |
157 |
265 |
209 |
196 |
353 |
262 |
|
|
VSL |
539 |
706 |
629 |
412 |
608 |
538 |
|
|
VSW |
529 |
715 |
612 |
421 |
617 |
525 |
|
|
OVL |
176 |
284 |
231 |
98 |
176 |
140 |
|
|
OVW |
176 |
274 |
234 |
98 |
186 |
143 |
|
|
MEL |
196 |
343 |
259 |
176 |
392 |
262 |
|
|
MEW |
304 |
490 |
368 |
157 |
480 |
304 |
|
|
ATL |
402 |
735 |
592 |
402 |
666 |
532 |
|
|
ATW |
470 |
637 |
534 |
176 |
372 |
305 |
|
|
PTL |
588 |
843 |
695 |
470 |
715 |
616 |
|
|
PTW |
392 |
539 |
485 |
206 |
431 |
299 |
|
|
EL |
115 |
125 |
119 |
101 |
126 |
117 |
|
|
EW |
65 |
74 |
71 |
61 |
77 |
72 |
|
|
FO |
812 |
1,132 |
968 |
763 |
1,279 |
1,050 |
|
|
U |
320 |
1,328 |
806 |
369 |
812 |
570 |
|
|
T |
2,312 |
3,862 |
2,911 |
3,173 |
4,895 |
3,682 |
|
|
BW/BL (%) |
11 |
17 |
14 |
9 |
12 |
11 |
|
|
FO/BL (%) |
12 |
16 |
14 |
11 |
17 |
14 |
|
|
U/BL (%) |
5 |
15 |
12 |
6 |
10 |
8 |
|
|
T/BL (%) |
36 |
47 |
42 |
47 |
55 |
50 |
References
- 1. Chai JY. Echinostomes in humans (Chapter 7). In Fried B, Toledo R, editors. The Biology of Echinostomes. New York, USA. Springer; 2009. p. 147-183.
- 2. Ahn YK, Kang HS. Development and cercarial shedding of Echinostoma hortense in the snail host Radix auricularia coreana
. J Wonju Med Col 1988;1:137-152.
- 3. Lee SH, Hwang SW, Sohn WM, Kho WG, Hong ST, Chai JY. Experimental life history of Echinostoma hortense
. Korean J Parasitol 1991;29:161-172. (in Korean).
- 4. Chai JY, Lee SH. Food-borne intestinal trematode infections in the Republic of Korea. Parasitol Int 2002;51:129-154.
- 5. Ryang YS, Ahn YK, Lee KW, Kim TS, Hhan MH. Two cases of natural human infection by Echinostoma hortense and its second intermediate host in Wonju area. Korean J Parasitol 1985;23:33-40. (in Korean).
- 6. Lee SK, Chung NS, Ko IH, Sohn WM, Hong ST, Chai JY, Lee SH. An epidemiological survey of Echinostoma hortense infection in Chongsong-gun, Kyongbuk Province. Korean J Parasitol 1988;26:199-206. (in Korean).
- 7. Ryang YS. Studies on Echinostoma spp. in the Chungju Reservoir and upper stream of the Namhan River. Korean J Parasitol 1990;28:221-233. (in Korean).
- 8. Chai JY, Hong SJ, Sohn WM, Lee SH, Seo BS. Studies on intestinal trematode in Korea XVI. Infection status of loaches with the metacercariae of Echinostoma hortense
. Korean J Parasitol 1985;23:18-23.
- 9. Sohn WM. Fish-borne zoonotic trematode metacercariae in the Republic of Korea. Korean J Parasitol 2009;47(suppl):103-113.
- 10. Sohn WM, Na BK, Cho SH, Ju JW. Infection status of Isthmiophora hortensis metacercariae in dark sleepers, Odontobutis species, from some water systems of the Republic of Korea. Korean J Parasitol 2018;6:633-637.
- 11. Asada J. On a new echinostomatid trematode and its life history. Trans Jap Path Soc 1926;16:293-294. (in Japanese).
- 12. Park JT. A rat trematode, Echinostoma hortense Asada, from Korea. Keijo J Med 1938;9:283-286.
- 13. Yamaguti S. Studies on the helminth fauna of Japan. Part 27. Trematodes of mammals, II. Jpn J Med Sci 1939;1:131-151.
- 14. Seo BS, Rim HJ, Lee CW. Studies on the parasitic helminths of Korea I. Trematodes of rodents. Korean J Parasitol 1964;2:20-26.
- 15. Seo BS, Rim HJ, Lee CW, Yoon JS. Studies on the parasitic helminths of Korea II. Parasites of the rat, Rattus norvegicus Erxl. in Seoul, with the description of Capillaria hepatica (Bancroft, 1893) Travassos (1915). Korean J Parasitol 1964;2:55-62.
- 16. Seo BS, Cho SY, Hong ST, Hong SJ, Lee SH. Studies on parasitic helminths of Korea V. Survey on intestinal trematodes of house rats. Korean J Parasitol 1981;19:131-136.
- 17. Cho SY, Kang SY, Ryang YS. Helminthes infections in the small intestine of stray dogs in Ejungbu City, Kyunggi do, Korea. Korean J Parasitol 1981;19:55-59. (in Korean).
- 18. Chen HT. Fauna Sinica. Platyhelminthes, Trematoda, Digenea (I). Beijing, China. Science Press; 1985. p. 333-497 (in Chinese).
- 19. Fan SQ, Sun MF. Echinostoma hortense. Bull Harbin Medl Univ 1989;23:161. (in Chinese).
- 20. Lee SH, Sohn WM, Chai JY.
Echinostoma revolutum and Echinoparyphium recurvatum recovered from house rats in Yangyang-gun, Kangwon-do. Korean J Parasitol 1990;28:235-240.
- 21. Sohn WM, Chai JY. Infection status with helminthes in feral cats purchased from a market in Busan, Republic of Korea. Korean J Parasitol 2005;43:93-100.
- 22. Sohn WM, Na BK, Song HJ, Kim CM, Nam GJ. Intestinal helminthic infections in striped field mice, Apodemus agrarius, from two southern regions of Korea. Korean J Parasitol 2014;52:419-423.
- 23. Sohn WM, Na BK, Shin SS. New definitive hosts and differential body indices of Isthmiophora hortensis (Digenea: Echinostomatidae). Korean J Parasitol 2017;55:287-294.
- 24. Nguyen LAT, Madsen H, Ha DT, Hoberg E, Dalsgaard A, Murrell KD. Evaluation of the role of rats as reservoir hosts for fishborne zoonotic trematodes in two endemic northern Vietnam fish farms. Parasitol Res 2012;111:1045-1048.
- 25. Shin SS, Oh DS, Ahn KS, Cho SH, Lee WJ, Na BK, Sohn WM. Zoonotic intestinal trematodes in stray cats (Felis catus) from riverside areas of the Republic of Korea. Korean J Parasitol 2015;53:209-213.
- 26. Kostadinova A, Gibson DI.
Isthmiophora Lühe, 1909 and Euparyphium Diet, 1909 (Digenea: Echinostomatidae) redefined, with comments on their nominal species. Syst Parasitol 2002;52:205-217.
- 27. Fuhrmann O. Neue Trematoden. Centralblatt für Bakteriologie und Parasitenkunde, Erste Abteilung 1904;37:58-64. (in German).
- 28. Kontrimavichus VL. Helminth fauna of Mustelidae from the Far East. Trudy Gel’mintologicheskoi Laboratorii. Akademiya Nauk 1963;13:26-47. (in Russian).
- 29. Kontrimavichus VL. Helminths of mustelids and trends in their evolution. New Delhi, India. Amerind Publishing Co; p. 1-607.
- 30. Karyakarte PP. On a species of Euparyphium (Trematoda: Echinostomatidae) recorded for the first time from the otter, Lutra lutra in India. Riv Parassitol 1968;29:227-228.
- 31. Nguyen TL. Three new species of trematodes from vertebrates in the Democratic Republic of Viet Nam. Materialy Nauchnoy Konferentsii Vsesoyuznogo Obschchestva Gel’mintologov, Part 1 1969;200-206. (in Russian).
- 32. Hoberg EP, Henny CJ, Hedstrom OR, Grove RA. Intestinal helminths of river otters (Lutra canadensis) from the Pacific Northwest. J Parasitol 1997;83:105-110.
- 33. Choe S, Lee D, Park H, Oh M, Jeon HK, Lee Y, Na KJ, Kim Y, Lee H, Eom KS. Three echinostome species from wild birds in the Republic of Korea. Korean J Parasitol 2014;52:513-520.
- 34. Kostadinova A. Family Echinostomatidae Looss, 1899. In Jones A, Bray RA, Gibson DI, editors. Keys to the Trematoda. 2:London, UK. CABI Publishing and the Natural History Museum; 2005. p. 9-64.
- 35. Sahasrabunde VK, Shah HL. On the trematodes: Euparyphium inerme (Fuhrmann, 1904) (Echinostomatidae) and Haplorchis taichui (Nishigori, 1924) Witenberg, 1930 (Heterophyidae) in Indian dogs. Indian J Helminthol 1967;19:56-63.
- 36. Chertkova AN. Helminth fauna of Gazella subguttrosa
. Sbornik Rabot po Gel’mintologii posvyashchen 90-letiyu sodnya rozhdeniya Akademika K.I. Skrjabina. Moscow, Kolos. 1971. p. 436-440 (in Russian).
- 37. Skrjabin KI, Bashkirova EY. Family Echinostomatidae Dietz, 1909. Osnovy Trematodologii 1956;12:53-930. (in Russian).
- 38. Beaver PC. Studies on the life history of Euparyphium melis (Trematoda: Echinostomatidae). J Parasitol 1941;27:35-44.
- 39. Lumsden RD, Zischke JA. Seven trematodes from small mammals in Louisiana. Tulane Stud Zool 1961;9:87-98.
- 40. Nugaraitė D, Mažeika V, Paulauskas A. Helminths of mustelids (Mustelidae) in Lithuania. Biologija 2014;60:117-125.
- 41. Korol EN, Varodi EI, Kornyushin VV, Malega AM. Helminths of wild predatory mammals (Mammalia, Carnivora) of Ukraine. Trematodes. Vestnik Zoologii 2016;50:301-308.
- 42. 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).
- 43. Choe S, Lee D, Park H, Jeon HK, Lee Y, Kim E, Na KJ, Eom KS. Two echinostome species, Pegosomum bubulcum and Nephrostomum ramosum (Digenea: Echinostomatidae) from an Eastern cattle egret, Bubulcus ibis coromandus, in Republic of Korea. Korean J Parasitol 2016;54:485-496.
- 44. Choe S, Lee D, Park H, Jeon HK, Lee Y, Na KJ, Park SR, Eom KS. A case of chaunocephalosis by Chaunocephalus ferox (Digenea: Echinostomatidae) in an oriental white stork, Ciconia boyciana, in Korea. Korean J Parasitol 2016;54:659-665.
- 45. Sohn WM, Na BK. Infections with digenetic trematode metacercariae in freshwater fishes from two visiting sites of migratory birds in Gyeongsangnam-do, Republic of Korea. Korean J Parasitol 2019;57:273-281.
