Discovery of natural infection by Metagonimus hakubaensis Shimazu, 1999 (Trematoda: Heterophyidae) in Japanese water shrews (Chimarrogale platycephala) in Japan.

A total of 611 preserved adult Metagonimus spp. specimens recovered from 32 of 53 Japanese water shrews (Chimarrogale platycephala) that had previously been collected in Aomori Prefecture between June 1994 and August 1996, were examined in this study. Morphological examination revealed that 603 of these flukes were identical to M. hakubaensis Shimazu, 1999, and that the others were M. takahashii Suzuki, 1930 (n=4), M. otsurui Saito et Shimizu, 1968 (n=2), and M. miyatai Saito et al., 1997 (n=2). Each of the 32 Japanese water shrews infected with M. hakubaensis contained between 1 and 83 flukes. This is the first record of the natural final host for M. hakubaensis, since this fluke species was described.

Metagonimus hakubaensis Shimazu, 1999 was originally described from laboratory rats that had been orally administered metacercariae recovered from sand lampreys (Lethenteron reissneri (Dybowski)) from Nagano Prefecture, Japan [6]. Trematodes in the genus Metagonimus occur naturally in the small intestines of a variety of mammals and birds. In Japan, natural infections of M. yokogawai (Katsurada, 1912), M. takahashii Suzuki, 1930 and M. miyatai Saito et al., 1997, have been reported in dogs, cats, pigs, raccoon dogs, weasels, martens, red foxes, Japanese water shrews, thrushes, kites, gulls and humans [2, 3]. Although M. otsurui Saito et Shimizu, 1968 and M. katsuradai Izumi, 1935 have been recovered from Japanese water shrews and stray dogs, respectively [5, 7], the natural final host of M. hakubaensis has remained unknown. We therefore conducted morphological examinations of preserved Metagonimus spp. specimens that had been recovered from Japanese water shrews (Chimarrogale platycephala (Temminck)) collected in Aomori Prefecture approximately 20 years previously.

Between June 1994 and August 1996, a total of 53 water shrews were collected from three sites (Temmabayashi, Kamikita and Sitinohe) in eastern Aomori Prefecture, Japan. The water shrews were examined for intestinal flukes, which were fixed in 70% alcohol between a glass slide and a cover slip, stained with alum carmine and mounted in Canada balsam. The stained specimens were preserved in our laboratory until morphological examination.

A total of 611 adult Metagonimus spp. were recovered from the intestines of 32 water shrews. Of these flukes, 603 were identical to M. hakubaensis, and the others were identified as M. takahashii (n=4), M. otsurui (n=2) and M. miyatai (n=2). Metagonimus hakubaensis was found in all of the infected animals, and the number of flukes recovered from each animal ranged from 1 to 83. Representative specimens of M. hakubaensis were deposited in the collection of the Meguro Parasitological Museum (MPM Coll. No. 20948). In addition, Plagiorchis fuji and Echinostoma hortense were detected in 38 and 2 water shrews, respectively. Although 3 intestinal trematode species belonging to genus Macroorchis (Ma. chimarrogalus, Ma. elongatus and Ma. spinulosus) have been reported from Japanese water shrews in eastern Japan, these flukes were not found in this study [4]. The morphology of the M. hakubaensis specimens recovered from the water shrews is described below.

Body elongated oval or elliptical, flattened dorsoventrally, 600–760 µm long, maximum width of posterior half measuring 248–320 µm (Fig. 1A and 1B). Body surface covered with minute scale-like spines, which are conspicuous on anterior half of body. Oral sucker subterminal, transversely elliptical, measuring 60–74 by 56–72 µm. Prepharynx short. Pharynx subglobular, 24–36 µm long, 26–38 µm wide. Esophagus 50–92 µm long, bifurcating at approximately anterior one-fifth of body. Two ceca extend laterally, terminating at anterior margin of right testis and posterior margin of left testis; ceca do not extend over testes to the posterior end of body (Fig. 1C and 1D). Ventral sucker, with adjoined genital atrium, situated at middle of anterior half of body, deflecting to right of median line with the long axis inclined obliquely or directed transversely; ventral sucker is elliptical in shape, measuring 56–72 by 40–52 µm, slightly smaller than or equal to oral sucker in size (size ratio of ventral sucker to oral sucker 0.85–1.16: 1). Testes round to elliptical, lying obliquely at posterior end of body; right testis close to posterior extremity, measuring 104–150 by 70–110 µm; left testis 100–144 by 68–114 µm. Ovary round or oval, 66–90 by 62–70 µm in size, situated at middle of body. Seminal vesicle transversely elliptical, located in front of ovary, varying in size, 70–150 by 30–60 µm. Seminal receptacle oval or kidney-shaped, 60–112 by 40–100 µm, located slightly behind right side of ovary. Uterus occupying almost all available space in midbody from ventral sucker to testes, not extending to posterior extremity between both testes. Vitellaria extending in lateral and median fields from ovary to midlevel of left testis. Eggs yellowish-brown, oval to elliptical in shape, with a distinct operculum, embryonated; eggs in uterus measuring 28–32 by 16–20 µm.

Fig. 1.

Metagonimus hakubaensis recovered from a Japanese water shrew. Bar=100 µm. (A, B) ventral view of entire body and (C, D) ventral view of posterior region.

According to Shimazu [6], M. hakubaensis is closely similar to M. otsurui and M. katsuradai in that the oral sucker is larger than the ventral sucker, but differs from these 2 species in that neither the ceca nor the vitellaria extend posteriorly beyond the right testis, and the uterus hardly enters the post-testicular region. The morphological findings of the specimens recovered from water shrews in this study agree very well with previously published characteristics of M. hakubaensis [6]. In addition, the morphometric measurements of the flukes recovered from the water shrews were similar to those recovered from experimentally infected rats (Table 1).

Table 1.

Comparison of measurements of Metagonimus hakubaensis from 2 different hosts (in µm)

	Present authors	Shimazu (1999)
Host	Water shrew	Rata)
No. of specimens	20	20b)
Body length	600–760	490–640
width	248–320	280–420
Oral sucker	60–74 × 56–72	58–78 × 43–58
Ventral sucker	56–72 × 40–52	51–70 × 39–51
Pharynx	24–36 × 26–38	27–35 × 19–31
Esophagus	50–92	20–94
Left testis	100–144 × 68–114	100–150 × 70–120
Right testis	104–150 × 70–110	100–160 × 80–120
Ovary	66–90 × 62–70	60–90 × 70–100
Seminal vesicle	70–150 × 30–60	80–136 × 40–64
Seminal receptacle	60–112 × 40–100	60–160 × 40–100
Eggs	28–32 × 16–20	28–34 × 16–20

a) Rats were experimentally infected with the metacercariae of M. hakubaensis collected from sand lampreys. b) Flukes from day 22 post-infection.

The Japanese water shrew lives in rapidly flowing streams, small rivers and ponds, where it swims actively to capture prey, such as crabs, shrimps, tadpoles, small fishes and aquatic insects [1]. In previous surveys of metacercarial infections in fresh water fishes (unpublished data), we found an M. hakubaensis-like species in sand lampreys collected at Temmabayashi (one of the sites where M. hakubaensis was detected in water shrews) in Aomori Prefecture. It is thus possible that the water shrews may have become infected with M. hakubaensis by preying on sand lampreys. Since trematodes in the genus Metagonimus infect a wide range of mammals and birds, further studies are necessary in order to clarify the final hosts of M. hakubaensis. This is the first known record of a natural final host for M. hakubaensis, since this fluke species was described.