Intestinal Parasites among Wild Rodents in Northern Gangwon-do, Korea

Since rodents can be natural final hosts of intestinal trematodes, several studies have been performed on parasitic infections among rodents. For example, Neodiplostomum seoulense, originally recovered from a house rat in 1964, was subsequently discovered in a man with epigastric pain, suggesting the role of rodents as a reservoir host for this trematode infection [1]. Moreover, echinostomes were reported in rats collected in Seoul, Yangyang-gun (Gangwon-do), Goyang-gun (Gyeonggi-do), Iksan-gun (Jeollabuk-do), and northern Gyeonggi-do near the demilitarized zone (DMZ), the Republic of Korea (=Korea) [2-5].

The prevalence of Plagiorchis muris, recently proved to be a human intestinal trematode, had also been surveyed in endemic areas. The adult worms of P. muris were discovered in rodents from Hadong-gun (Gyeongsangnam-do), Yongin-si (Gyeonggi-do), and Yangyang-gun (Gangwon-do), and 5.3% of Apodemus agrarius were infected with P. muris in northern Gyeonggi-do, near the demilitarized zone [3,6,7]. Outside of Korea, it was reported that the overall prevalence of P. muris was 16.9% in the wood mouse of North Yorkshire, UK [8]. However, most Korean studies were performed on house rodents except for some studies performed from DMZ [5,7]. Considering the importance of sylvatic rodents as the reservoir host for intestinal flukes, more surveys should be performed on wild rodents in Korea. This study was initiated to determine the geographical patterns of natural parasite infections among small mammals and focused on the patterns and rates of intestinal parasite infections among the wild rodents from northern Gangwon-do (Province).

A total of 56 rodents were live-captured from 3 sites of northern Gangwon-do, i.e., Gaojak-2-ri, Nam-myon, Yanggu-gun (site 1), Jukgok-ri, Yanggu-eup, Yanggu-gun (site 2), and Gaa-ri, Inje-eup, Inje-gun (site 3) by using Sherman traps (3×3.5×9 folding traps; H.B. Sherman, Tallahassee, Florida, USA) baited with peanut butter between saltine crackers. The captured rodents included the striped-field mouse, A. agrarius (n=43), Korean wood mouse, Apodemus peninsulae (n=11), Red-backed vole, Myodes regulus (n=1), and squirrel (n=1). Animal trapping was performed during the summer season (July and August) of the year 2011. Captured animals were euthanized in accordance with the approved animal use protocol under biosafety level 3 (BSL-3) laboratory conditions. The whole intestine to the end of the rectum was removed and preserved in 70% alcohol till the time of examination. The gastrointestinal contents were opened in a Petri dish containing distilled water, and all helminths were collected under a dissecting microscope (×10). Finally, worms were examined under a light microscope for species identification.

In site 1 (Yanggu-gun, Gaojak-ri), 7 out of 9 (77.8%) captured A. agrarius were found to be infected with helminths. In site 2 (Yanggu-gun, Jukgok-ri), all captured 11 A. agrarius and 7 A. peninsulae were found to be infected with helminths. In site 3 (Inje-gun, Gaa-ri), 15 out of 23 (65.2%) A. agrarius were found to be infected with helminths. No parasite was recovered from the red-backed vole and the squirrel. The infection rates of each intestinal parasite in A. agrarius and A. peninsulae are summarized in Table 1. Briefly, 72.1% of A. agrarius and 63.6% of A. peninsulae were found to be infected with various species of intestinal parasites. In A. agrarius, hookworm infection rate (41.9%; 18/43) was the highest, followed by Syphacia spp. (14.0%) and ascarids (11.6%) among the nematodes. In case of trematodes, 2 specimens of P. muris were collected and no other species of trematodes were found (Fig. 1). In addition, 2 species of cestodes, i.e., Hymenolepis nana and Hymenolepis diminuta, were collected from A. agrarius. The species of 2 nematodes and 2 cestodes were unable to identify. In A. peninsulae, the overall nematode infection rate (63.6%) was similar to that of A. agrariuis except the fact that the proportion of hookworms among the nematodes was relatively higher in A. peninsulae than in A. agrarius because of the absence of ascarids and small numbers of Syphacia spp. in A. peninsulae. Unlike A. agrarius, only 1 Echinostoma hortense was collected as a trematode and no other species were found. Whereas H. nana was also collected from A. agrarius, H. diminuta was the only cestode found in A. peninsulae.

Table 1.

Infection rates of intestinal parasites in Apodemus agrarius and Apodemus peninsulae caught from 3 sites of Yanggu-gun and Inje-gun in northern Gangwon-do, Republic of Korea

Fig. 1

(A) An adult worm of Plagiorchis muris recovered from a striped field mouse, Apodemus agrarius. Bar=200 µm. (B) An adult of Echinostoma hortense recovered from a Korean wood mouse, Apodemus peninsulae. Bar=200 µm. OS, oral sucker; VS, ventral sucker; O, ovary; T, testis; VT, vitellaria; HC, head crown.

This is the first report on intestinal parasites among wild rodents in Gangwon-do, suggesting that wild rodents might play a role in maintaining the sylvatic cycle of some trematodes. Among them, P. muris is a small intestinal fluke (2.9-3.0 mm long) and there have been several reports on human infections [9,10]. According to a previous survey performed in a northern part of Korea, the majority (83.3%) of A. agrarius were infected with P. muris [2]. A. agrarius is still strongly suggested as an important reservoir of P. muris in northern parts of Korea [7] and in this survey, P. muris was also collected from A. agrarius although the infection rate was relatively low. In addition, an adult worm of E. hortense was recovered from A. peninsulae, proving the potential of A. agrarius as the natural definitive host in northern Gangwon-do.

H. nana, a dwarf tapeworm, is most common in temperate zone including the Korean peninsula. For a long time, it had been a relatively common cestode infection in Korea, especially in children. The nationwide survey in 1986 revealed that the egg positive rate of H. nana was 0.22%, but a review of zoonotic parasites in Korea also indicated very low prevalence of H. nana infection in comparison to other zoonotic cestodes like Taenia spp. [11,12]. However, the possibility of H. nana infection has still been present as seen in the case of a 40-year-old man [13], and symptoms can attend heavy worm burdens. Although H. diminuta is also known as a zoonotic cestode like H. nana, human infection cases by H. diminuta was almost absent in Korea after the first case report in 1966 [12,14]. However, in this survey, considerable infection rates of H. diminuta were shown in both A. agrarius (27.9%) and A. peninsulae (54.5%), still implying the possibilities of zoonotic infection by this cestode along with H. nana.

Taken together, the increased demands for leisure activities in northern Gangwon-do, Korea might provide the chance of opportunistic parasite infections around the areas of this survey. Furthermore, 2 major lakes (Paro-ho and Soyang-ho) which provide many attractive basins for freshwater fishing are located near from the survey sites. Therefore, seasonal and further comprehensive surveys on natural parasite infections in these areas are needed for an effective control of human infections by intestinal flukes and tapeworms.