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Original Article

Intestinal Helminthic Infections in Striped Field Mice, Apodemus agrarius, from Two Southern Regions of Korea

Woon-Mok Sohn1, Byoung-Kuk Na1, Hyeon-Je Song2,†, Chung-Mo Kim2, Gi-Jin Nam3
The Korean Journal of Parasitology 2014;52(4):419-423.
Published online: August 29, 2014

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Corresponding author (wmsohn@gnu.ac.kr)

†Present address: Department of Clinical Pathology, Gwangju Health University, Gwangju 506-701, Korea.

• Received: February 23, 2014   • Revised: May 14, 2014   • Accepted: June 24, 2014

© 2014, Korean Society for Parasitology and Tropical Medicine

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  • The present study was performed to know the infection status of intestinal helminths in a most common species of field mice, Apodemus agrarius, from 2 southern regions of Korea. Total 133 and 103 mice were collected by the mouse trap in Hapcheon-gun, Gyeongsangnam-do and Gurye-gun, Jeollanam-do, respectively, from July 2005 to June 2006. The small intestine of each mouse was resected and longitudinally opened with a pair of scissors. The intestinal contents were washed with 0.85% saline until the supernatant became clear. Helminths were collected with naked eyes or under a stereomicroscope from the sediment of the intestinal content. More than 11 species of helminths (4 nematode spp., 5 trematode spp., and 2 cestode spp.) were recovered. Among these, heligmosomoid nematodes (97.5%) was the most highly and heavily infected species. As the members of trematodes, Plagiorchis muris, Brachylaima sp., Echinostoma hortense, Echinostoma cinetorchis, and unidentified echinostome larvae were found in the small intestines of 35 (14.8%), 12 (5.1%), 6 (2.5%), 1 (0.4%), and 1 (0.4%) mice respectively. Two species of tapeworms, Hymenolepis nana and Hymenolepis diminuta were also detected in 79 (33.5%) and 21 (8.9%) mice, respectively. Conclusively, heligmosomoid nematodes were the most prevalent (dominant) species among more than 11 helminth species detected, and Brachylaima sp. fluke is newly added in the list of intestinal trematodes in Korea.
  • Key words: Intestinal helminth, striped field mouse, Apodemus agrarius, southern region of Korea
Studies on rodent parasites of medical and veterinary importance have been performed to prevent transmission of diseases to humans and domestic animals. A variety of rodent species were investigated in various regions of the world [1,2,3]. The striped field mouse, Apodemus agrarius, is the most dominant species and the agricultural scourge in the Republic of Korea (=Korea). This mouse species is widely distributed in rural areas, agricultural fields, and forest in small mountains. It causes a great deal of economic loss in agricultural products and also acts as the natural transmitter for zoonotic parasites as well as pathogens like tularemia, leptospirosis, and hemorrhagic fever [4].
Rodent parasites have been investigated by many workers in Korea. In the 1930's, Cysticercus fasciolaris, Capillaria hepatica, Hymenolepis diminuta, Hymenolepis nana, and Echinostoma hortense were reported [5,6,7]. Subsequently, a variety of helminth species were detected and described from various species of rodents in the 1960's [8,9,10]. Later, Seo et al. [11] found 6 trematode species in 170 house rats collected from 13 localities in Korea. In the 1990's, several species of helminths were also detected in rodent hosts from some localities including Gangwon-do through 3 additional surveys [12,13,14].
Recently, Chai et al. [15,16] reported the infection status of Plagiorchis muris and echinostomes in the striped field mice from the northern Gyeonggi-do near the demilitarized zone (DMZ). It was also reported that the striped field mouse is a new definitive host for Neodiplostomum seoulense [17]. Lee et al. [18] surveyed 56 wild rodents from northern Gangwon-do to examine the infection status of intestinal helminths. Most of these surveys on rodent parasites were done in the northern regions of Korea, and little data are available on the helminth diversity among rodents in southern regions of Korea. Therefore, the present study was performed to provide preliminary data on the intestinal helminth fauna in striped field mice inhabiting 2 southern regions, Hapcheon-gun, Gyeongsangnam-do and Gurye-gun, Jeollanam-do, Korea.
From July 2005 to June 2006, we collected the striped field mice, A. agrarius, once every month in the 2 southern regions, Hapcheon-gun and Gurye-gun. Sherman's rodent live traps were set at 11 outdoor places in the 2 southern regions afternoon and were collected at the early morning of the next day. The collected mice were anesthetized and killed after taking samples for preventive studies of febrile diseases in 2 laboratories of Gyeongsangnam-do and Jeollanam-do Institutes of Health and Environment, in Changwon-si and Gwangju-si, respectively, Korea. Intestines of each mouse were extracted from the abdominal cavity after dissection, preserved in a specimen bottle with 0.85% saline, and then transported to the laboratory in the Department of Parasitology and Tropical Medicine, Gyeongsang National University School of Medicine, Jinju, Korea.
The small intestine of each mouse was longitudinally opened with a pair of scissors. The intestinal contents were washed with 0.85% saline until the supernatant became clear. The helminthic worms were collected with naked eyes or under a stereomicroscope from the sediment of the intestinal content. After applying specific clearing and staining techniques, the collected helminths were identified using appropriate systematic keys, and each of them was counted to get hold of the infection rates and densities per mouse.
Infection rates of each helminth species
More than 4 species of nematodes, i.e., heligmosomids, Syphacia sp., ascarids, and hookworms were detected from 230 (97.5%), 12 (5.1%), 6 (2.5%), and 1 (0.4%) striped field mice, respectively. As the trematodes, Plagiorchis muris, Brachylaima sp., Echinostoma hortense, Echinostoma cinetorchis, and unidentified echinostome larvae were found in 35 (14.8%), 12 (5.1%), 6 (2.5%), 1 (0.4%), and 1 (0.4%) mice, respectively. H. nana and H. diminuta were detected from 79 (33.5%) and 21 (8.9) mice, respectively. Helminth species recovered and their infection rates by surveyed areas were presented in Table 1.
Infection status of heligmosomids by surveyed areas and months
Heligmosomid nematodes were recovered from 129 (97.0%) mice from Hapcheon-gun, Gyeongsangnam-do, and their average number was 97.5 per mouse infected. In mice from Gurye-gun, Jeollanam-do, heligmosomids were recovered from 101 (98.1.0%) mice, and their average number was 52.2 per infected mouse. The monthly results of heligmosomids recovery are shown in Tables 2 and 3.
Infection status of trematodes
P. muris were collected in the small intestines of 26 (19.5%) and 9 (8.7%) mice from Hapcheon-gun and Gurye-gun, respectively, and their worm burdens were 9.9 and 1.9, respectively, per infected mouse. E. hortense were detected in 5 (3.8%) mice from Hapcheon-gun, and their worm burdens were 5.0 per infected mouse. A total of 64 Brachylaima sp. flukes were found in 12 (11.7%) mice from Gurye-gun, and their worm burdens were 5.3 per infected mouse (Table 4).
Brief description of Brachylaima sp. (Digenea: Brachylaimidae)
Body elongate with spinose tegument and 4,422 by 1,000 in average size (all measurement unit is µm). Oral sucker subterminal and 299 by 354 in size. Prepharynx very short. Pharynx muscular and 176 by 236 in size. Esophagus absent. Intestinal ceca bifurcate directly at the pharynx and extend parallel to lateral margins to nearly posterior end of the body forming undulations. Ventral sucker (417 by 427) slightly larger than oral sucker and located at about anterior 1/4 of body. Ovary transversely oval or elliptical, 212 by 315 in size, and located slightly dextral between 2 testes. Testes round to irregular in shape, with smooth or slightly lobulated margins, and the anterior one (380 by 423) slightly larger than the posterior one (331 by 380). Vitelline follicles distribute laterally or extracecally from the slightly lower level of pharynx to the level of anterior testis or ovary. Uterus consists of many loops with numerous eggs, and distributes intracecally from the level of pharynx to the level of anterior testis. Eggs small, operculate, and 24.8 by 14.1 in average size. The morphological characteristics will be described separately as a faunistic study in the near future.
In the present study, more than 11 species of helminths were recovered from 236 striped field mice examined. Among these, heligmosomid nematodes were most prevalent. Total 230 (97.5%) mice were infected with 77.6 heligmosomids in average. The prevalence rates were more or less similar in mice from 2 regions, but worm burdens were higher in mice from Hapcheon-gun, Gyeongsangnam-do. Unfortunately, we could not taxonomically define their generic and species names. On the other hand, Seo et al. [10] detected Heligmosomum sp. in the intestines of 7 wild rodent species and Heligmosomoides sp. in 3 specie from 4 northern regions, Cheolwon, Geumwha, Pocheon, and Paju, in Gangwon-do and Gyeonggi-do respectively [10]. They also described brief morphological characteristics of 2 heligmosomids, Heligmosomum sp. and Heligmosomoides sp., for the first time in Korea [10].
Seo et al. [10] recorded 7 rodent species, i.e., A. agrarius, Rattus norvegicus, Rattus alexandrinus, Mus musculus yamashinai, Crocidura russula, Microtus fortis, and Cricetulus triton nester, as the hosts of Heligmosomum sp. and they also listed 3 species, i.e., A. agrarius, R. norvegicus and M. fortis, as the hosts of Heligmosomoides sp. in Korea. Out of 300 rodents in 7 species examined, the striped field mouse, A. agrarius, was the dominant species (73.0%) and revealed 14.6% and 13.2% prevalence rates of Heligmosomum sp. and Heligmosomoides sp., respectively. The prevalence rate (97.5%) of heligmosomids in this study was much higher than that of Seo et al. [10]. The difference of infection rates with these nematodes may be closely related to the inhabitation environment of rodent hosts. Survey areas in this study were 2 southern regions, Hapcheon-gun and Gurye-gun, whereas those in Seo et al. [10] were 5 northern regions, Cheolwon, Geumwha, Cheongpyeong, Pocheon, and Paju in Gangwon-do and Gyeonggi-do.
Seo et al. [10] found 8 species of nematodes, i.e., Nippostrongylus muris Syphacia obvelata, Heterakis spumosa, Protospirura muris, Heligmosomum sp., Heligmosomoides sp., Rictularia sp., and Gongylonema sp., in 219 A. agrarius from 5 northern regions of Korea [10]. Yong et al. [13] detected 3 species of nematodes, i.e., N. muris, S. obvelata, and Gongylonema sp., in 85 A. agrarius from Goyang-gun, Gyeonggi-do and Iri-si and Iksan-gun, Jeollabuk-do [13]. In aforementioned 2 studies, N. muris was the dominant species. However, in the present study, more than 4 nematode species, i.e., heligmosomids, S. obvelata, ascarids, and hookworms, were detected from 236 A. agrarius, and heligmosomids was the dominant one. Collectively, it is confirmed that various species of nematodes are inhabited in the gastrointestinal tract of striped field mice in Korea, and their infection rates and worm burdens are much higher than those of trematodes and cestodes.
As the trematodes inhabit in rodents, about 10 species, i.e., E. hortense, E. cinetorchis, Echinostoma revolutum, Echinoparyphium recurvatum, Echinochasmus japonicus, Euparyphium murinum, P. muris, N. seoulense, Clonorchis sinensis, and Metagonimus yokogawai, were reported in Korea [7,8,9,11,12,13,15,16,17,18]. Since E. hortense was reported for the first time in 1938 [7], E. cinetorchis, E. murinum, P. muris, and N. seoulense were added in the list of rodent trematodes by Seo et al. [8,9]. Seo et al. [11] detected 6 trematode species, i.e., E. hortense, E. cinetorchis, P. muris, N. seoulense, C. sinensis, and M. yokogawai, from 170 house rats. Lee et al. [12] also found 6 trematode species, i.e., E. hortense, E. cinetorchis, E. revolutum, E. recurvatum, P. muris, and N. seoulense in 2 house rats from Yangyang-gun, Gangwon-do [12]. Yong et al. [13] detected only 1 specimen of E. japonicus from a striped field mouse [13]. Recently, Chai et al. [15,16,17] reported the infection status of P. muris, N. seoulense, and echinostomes in 1,366 striped field mice from northern Gyeonggi-do near the demilitarized zone. When we analyzed the infection status of rodent trematodes reported previously, 4 species, i.e., E. hortense, E. cinetorchis, P. muris, and N. seoulense, are known to be widely distributed in Korea. However, Brachylaima sp. had not been reported in Korea before this study. Therefore, we will try to record this as a new trematode fauna of Korea in the near future.
Total 5 species of rodent tapeworms, i.e., C. fasciolaris, H. diminuta, H. nana, Raillietina coreensis, and Paranoplocephala sp., have been reported in Korea [5,6,10,13,14]. Since C. fasciolaris was reported for the first time as the rodent tapeworm by Nakamura and Kobayashi in Korea [5], H. diminuta and H. nana were listed by Ogura [6], and R. coreensis and Paranoplocephala sp., were added by Seo et al. [10]. Among 5 tapeworm species, C. fasciolaris was most frequently found from the rodent hosts [5,9,10,13,14]. However, this larval tapeworm was not detected in the present study, because we examined only the small intestines. If we examined the liver of mice as well, C. fasciolaris may have been recovered together with H. diminuta and H. nana in the present study.
Trematodes and cestodes inhabited in the rodent hosts can be, unlike nematodes, zoonotic pathogens. Especially, E. hortense, P. muris, N. seoulense, H. diminuta, and H. nana, widely prevalent among wild rodents in Korea, are commonly infected in humans also, and they are able to act as the reservoir host for human infections. However, among the nematodes, Capillaria hepatica is potentially a zoonotic pathogen to humans. Seo et al. [9] detected this nematode from 286 (88.0%) house rats, and a human (child) case by this zoonotic nematode infection was already reported in Korea [19]. Accordingly, we should pay attention to wild rodents acting as the reservoir host of trematode and cestode infections as well as hepatic capillariasis.
Conclusively, the fauna and infection status of helminths in the striped field mouse, A. agrarius, from 2 southern regions of Korea were partly revealed by the present study. The most prevalent (dominant) species, heligmosomoid nematodes, should be clarified in generic and species levels, and Brachylaima sp., newly added in the list of intestinal fluke, should also be named in the near future.
National Institute of Health

We have no conflict of interest related to this study.

This work was financially supported by a grant from the National Institute of Health (NIH, 2005, 2006), Korea, as a part of the Anti-Communicable Diseases Program: Control and Research Strategies against Tropical and Endemic Diseases. We thank Jung-A Kim and A-Ra Cho, Department of Parasitology and Tropical Medicine, Gyeongsang National University School of Medicine, Jinju, Korea, for their help in the recovery of worms.
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Table 1.
Recovery rates of helminths in the small intestines of Apodemus agrarius from Hapcheon-gun, Gyeongsangnam-do and Gurye-gun, Jeollanam-do, Korea
Table 1.
Helminth No. (%) of positive mice from
Hapcheona Guryeb Total
Nematodes
 Heligmosomids 129 (97.0) 101 (98.1) 230 (97.5)
 Syphacia obvelata 6 (4.5) 6 (5.8) 12 (5.1)
 Ascarid - 6 (5.8) 6 (2.5)
 Hookworm - 1 (1.0) 1 (0.4)
Trematodes
 Plagiorchis muris 26 (19.5) 9 (8.7) 35 (14.8)
 Echinostoma hortense 5 (3.8) 1 (1.0) 6 (2.5)
 Echinostoma cinetorchis 1 (0.8) - 1 (0.4)
 Unidentified echinostome larvae 1 (0.8) - 1 (0.4)
 Brachylaima sp. - 12 (11.7) 12 (5.1)
Cestodes
 Hymenolepis nana 51 (38.3) 28 (27.2) 79 (33.5)
 Hymenolepis diminuta 11 (8.3) 10 (9.7) 21 (8.9)

a133 and b103 mice were examined.

Table 2.
Quantitative results of heligmosomids recovery in Apodemus agrarius from Hapcheon-gun, Gyeongsangnam-do, Korea
Table 2.
Year month No. of mice examined No. (%) of mice infected No. of worms recovered
Total Range Average
2005
 July 17 16 (94.1) 983 12-236 61.4
 August 10 10 (100) 1,207 25-258 120.7
 September 11 11 (100) 1,435 7-316 130.5
 October 20 20 (100) 3,813 19-618 190.7
 November 9 9 (100) 648 25-259 72.0
2006
 January 12 11 (91.7) 533 1-135 48.5
 February 13 12 (92.3) 637 20-220 53.1
 March 7 6 (85.7) 280 13-75 46.7
 April 6 6 (100) 396 17-116 66.0
 May 5 5 (100) 452 19-208 90.4
 June 23 23 (100) 2,190 4-447 95.2
Total 133 129 (97.0) 12,574 1-618 97.5
Table 3.
Quantitative results of heligmosomids recovery in Apodemus agrarius from Gurye-gun, Jeollanam-do, Korea
Table 3.
Year month No. of mice examined No. (%) of mice infected No. of worms recovered
Total Range Average
2005
 July 18 18(100) 1,038 4-346 57.7
 August 6 6(100) 764 38-297 127.3
 September 10 10(100) 861 21-246 86.1
 October 5 5(100) 1,131 16-946 226.2
 November 9 9(100) 338 7-187 37.6
2006
 February 13 12 (92.3) 377 1-167 31.4
 March 9 9(100) 198 3-63 22.0
 April 18 18(100) 291 2-76 16.2
 May 15 14 (93.3) 271 5-55 19.4
Total 103 101 (98.1) 5,269 1-946 52.2
Table 4.
Quantitative results of trematode recovery in Apodemus agrarius from Hapcheon-gun, Gyeongsangnam-do and Gurye-gun, Jeollanam-do, Korea
Table 4.
Locality & Helminth No. (%) of mice infected No. of worms recovered
Total Range Average
Hapcheon-guna
 Plagiorchis muris 26 (19.5) 258 1-71 9.9
 Echinostoma hortense 5 (3.8) 25 1-18 5.0
Gurye-gunb
 Plagiorchis muris 9 (8.7) 17 1-3 1.9
 Brachylaima sp. 12 (11.7) 64 1-23 5.3

a133 and b103 mice were examined in each area.

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Intestinal Helminthic Infections in Striped Field Mice, Apodemus agrarius, from Two Southern Regions of Korea
Korean J Parasitol. 2014;52(4):419-423.   Published online August 29, 2014
DOI: https://doi.org/10.3347/kjp.2014.52.4.419
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Intestinal Helminthic Infections in Striped Field Mice, Apodemus agrarius, from Two Southern Regions of Korea
Korean J Parasitol. 2014;52(4):419-423.   Published online August 29, 2014
DOI: https://doi.org/10.3347/kjp.2014.52.4.419
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Intestinal Helminthic Infections in Striped Field Mice, Apodemus agrarius, from Two Southern Regions of Korea
Intestinal Helminthic Infections in Striped Field Mice, Apodemus agrarius, from Two Southern Regions of Korea
Helminth No. (%) of positive mice from
Hapcheona Guryeb Total Nematodes  Heligmosomids 129 (97.0) 101 (98.1) 230 (97.5)  Syphacia obvelata 6 (4.5) 6 (5.8) 12 (5.1)  Ascarid - 6 (5.8) 6 (2.5)  Hookworm - 1 (1.0) 1 (0.4) Trematodes  Plagiorchis muris 26 (19.5) 9 (8.7) 35 (14.8)  Echinostoma hortense 5 (3.8) 1 (1.0) 6 (2.5)  Echinostoma cinetorchis 1 (0.8) - 1 (0.4)  Unidentified echinostome larvae 1 (0.8) - 1 (0.4)  Brachylaima sp. - 12 (11.7) 12 (5.1) Cestodes  Hymenolepis nana 51 (38.3) 28 (27.2) 79 (33.5)  Hymenolepis diminuta 11 (8.3) 10 (9.7) 21 (8.9) Year month No. of mice examined No. (%) of mice infected No. of worms recovered
Total Range Average 2005  July 17 16 (94.1) 983 12-236 61.4  August 10 10 (100) 1,207 25-258 120.7  September 11 11 (100) 1,435 7-316 130.5  October 20 20 (100) 3,813 19-618 190.7  November 9 9 (100) 648 25-259 72.0 2006  January 12 11 (91.7) 533 1-135 48.5  February 13 12 (92.3) 637 20-220 53.1  March 7 6 (85.7) 280 13-75 46.7  April 6 6 (100) 396 17-116 66.0  May 5 5 (100) 452 19-208 90.4  June 23 23 (100) 2,190 4-447 95.2 Total 133 129 (97.0) 12,574 1-618 97.5 Year month No. of mice examined No. (%) of mice infected No. of worms recovered
Total Range Average 2005  July 18 18(100) 1,038 4-346 57.7  August 6 6(100) 764 38-297 127.3  September 10 10(100) 861 21-246 86.1  October 5 5(100) 1,131 16-946 226.2  November 9 9(100) 338 7-187 37.6 2006  February 13 12 (92.3) 377 1-167 31.4  March 9 9(100) 198 3-63 22.0  April 18 18(100) 291 2-76 16.2  May 15 14 (93.3) 271 5-55 19.4 Total 103 101 (98.1) 5,269 1-946 52.2 Locality & Helminth No. (%) of mice infected No. of worms recovered
Total Range Average Hapcheon-guna  Plagiorchis muris 26 (19.5) 258 1-71 9.9  Echinostoma hortense 5 (3.8) 25 1-18 5.0 Gurye-gunb  Plagiorchis muris 9 (8.7) 17 1-3 1.9  Brachylaima sp. 12 (11.7) 64 1-23 5.3
Table 1. Recovery rates of helminths in the small intestines of Apodemus agrarius from Hapcheon-gun, Gyeongsangnam-do and Gurye-gun, Jeollanam-do, Korea

a133 and b103 mice were examined.

Table 2. Quantitative results of heligmosomids recovery in Apodemus agrarius from Hapcheon-gun, Gyeongsangnam-do, Korea
Table 3. Quantitative results of heligmosomids recovery in Apodemus agrarius from Gurye-gun, Jeollanam-do, Korea
Table 4. Quantitative results of trematode recovery in Apodemus agrarius from Hapcheon-gun, Gyeongsangnam-do and Gurye-gun, Jeollanam-do, Korea

a133 and b103 mice were examined in each area.

Table 1.

Table 2.

Table 3.

Table 4.

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