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Natural Echinococcus multilocularis infection in a Norway rat, Rattus norvegicus, in southern Hokkaido, Japan
lnfernarionalfournalfor Parasitology Vol. 22, No. 5, pp. 681-684, 1992 Printed in Grew Brimin
OOZC-7519192 $5.00 + 0.00 Pergamon Press Lrd Q I992 Ausrralim Socieryfor Porosifology
RESEARCHNOTE NATURAL ECHINOCOCCUS MULTILOCULARIS INFECTION IN A NORWAY RAT, RATTUS NORVEGICUS, IN SOUTHERN HOKKAIDO, JAPAN MUNEHIRO OKAMOTO,*~ OSAMU FUJITA,* JIRO ARIKAWA,~ TSUTOMUKUROSAWA,§YUZABURO OKU* and MASAO KAMIYA* *Department
of Parasitology,
§The Institute
of Experimental
Faculty of Veterinary Medicine and $Institute of Immunological Science, Hokkaido University, Sapporo 060, Japan Animal Sciences, Osaka University Medical School, Suita-shi 565, Japan
(Received 23 March 1992; accepted 6 April 1992) AbStraCt~KAMOTO
M., FUJITA O., ARIKAWA J., KUROSAWA T., OKU Y. and KAMIYA M.
1992. Natural
Echinococcus multilocularis infection in a Norway rat, Rattus norvegicus, in southern Hokkaido, Japan. International Journalfor Parasitology 22: 681-684. Forty-two rats, Rattus norvegicus, captured at a garbage dump in southern Hokkaido, Japan, were examined, and one was found to be infected with Echinococcus multilocularis. The lesions were found in the liver, lung, mesenteric lymph nodes, greater omentum and also free in the abdominal cavity. No necrosis was observed in any of the lesions, and inflammatory reactions were mild. Protoscoleces were observed in the large liver cysts. A homogenate of these cysts, when transplanted into the abdominal cavity of three Mongolian gerbils and a rat, yielded numerous fully developed protoscoleces at 4-7 months post-inoculation. Judging from this, it is postulated that the rat could become a natural intermediate host for E. multilocularis in this area. INDEX KEY WORDS: Echinococcus multilocularis; Taenia taeniaeformis; Norway natural infection; intermediate host; protoscolex; Japan.
A wide range of mammals, including rodents, lagomorphs, insectivores and ungulates, have been reported as susceptible to infection with Echinococcus multilocularis eggs @myth, 1964). Arvicoline rodents, mainly of the genera Microtus and Clethrionomys, are the most important in the natural life cycle of E. multilocuZuris, so that in most endemic areas the natural cycle is completed between these rodents and two genera of foxes, Vulpes and Alopex (Rausch,
1986). Domestic dogs and cats are also important as a source of infection for humans, as they capture and eat infected wild voles in some hyperendemic foci such as St. Lawrence Island (Rausch, 1986). However, the source of infection for dogs and cats is more likely to be rats and house mice, because these rodents are commonly captured by such carnivores. Nevertheless, there arc very few reports on natural infection with E. mu/tiloculuris larvae in rats and mice (Ohbayashi, 1975). A natural case of infection in the rat has so far
tPresent address and address for correspondence: The Institute of Experimental Animal Sciences, Osaka University Medical School, Suita-shi 565, Japan.
rat; Rat&s norvegicus;
only been reported once, from Barabinskaya Step, in the Soviet Union, when four of 50 rats examined were infected (Lukashenko & Zorikhina, 1961). In these cases, however, no protoscoleces were observed. As for experimental infection, Webster and Cameron (1961) reported that five rats examined were all negative 16 and 36 weeks after being orally inoculated with E. multilocularis eggs. Thus, it has been considered that rats were resistant to infection with E. multilocularis eggs (Webster & Cameron, 196 I), and do not have an important role to play in the natural cycle of E. multiloculuris. Norway rats were captured alive by traps in October 1989 at a garbage dump in Kamiiso, Southern Hokkaido. Japan. Forty-two rats, with weights ranging from 30 to 305 g, and aged from I to 13 months, estimated from eye lens weight (Yabe, 1979) were examined. Rats were sacrificed under anesthesia, and the helminth parasites in the thoracic and abdominal viscera examined. Nodules and lesions which were difficult to identify were removed from organs and fixed in 10% neutral buffered formahn solution. These tissues were dehydrated in an ethanol series and paraffin sections of 5 pm thickness were made. Sections
682
M. OKAMOTOet al.
FIG. 1. Macroscopic appearance of E. multilocularis lesion in the liver of naturally infected Norway rat (arrow). Two white portions (arrowhead) are the cysts of T. taeniaeformis.
were stained with either hematoxylin+osin or periodic acid Schiff stain for histological examination. Three species of helminths, E. multilocularis (l/42), Taenia taeniaeformis (38/42) and Capillaria hepatica (16/42), were found. The latter two species only parasitized the liver. The infection rate of T. taeniaeformis was very high and the number of these cysts per rat was one to six. The size and developmental stage of T. taeniaeformis were various even in the same rat. Fifteen out of 16 rats infected with C. hepatica were simultaneously infected with T. taeniaeformis. One male rat, with a 305 g body weight and 10.4 months old, was infected with E. multilocularis. This rat was also infected with three cysts of T. taeniaeformis, and with C. hepatica. E. multilocularis lesions were found in the liver, lung, mesenteric lymph nodes, greater omentum and also free in the abdominal cavity. The liver lesions, 15-20 mm in diameter, were multivesicular and macroscopically seemed to be typical cysts of E. multilocularis (Fig. 1). In the largest cyst of this lesion, protoscolex formation was observed. Some of these protoscoleces possessed complete hooks, but suckers were not well defined in any protoscoleces observed (Fig. 2), indicating incomplete development. Many small cystic structures were found in the
FIG. 2. Protoscoleces from the liver lesion of naturally infected Norway rat.
mesenteric lymph nodes, greater omentum and abdominal cavity. In the lung, one lesion, 6 mm in diameter, was observed in the right lobe, and in the left, central and lateral lobes lesions 34 mm in diameter were found. Microscopically, cysts of assorted size, several micrometers to several millimeters, were seen in the liver lesion. In the large cysts, the laminated layer was
Research Note
FIG. 3. Liver lesion in naturally infected Norway rat, showing developing protoscoleces (arrow). Periodic acid Schickstain.
683
adventitial tissue of all cysts, inflammatory cellular reactions were mild despite fibrous proliferations being observed. No necrosis was observed even in the center of the cysts. Three Mongolian gerbils, ~er~o~es unguiculatus, and one Wistar rat, intraperitoneally inoculated with homogenate of E. multilocularis cysts from the naturally infected rat’s liver, were examined at 47 months post-inoculation. All animals were infected and numerous morpholo~cally normal fully developed protoscoleces were observed (Fig. 5). In Hokkaido, spontaneous infection with E. multilocularis has been reported not only from rodents but also pigs and horses (Sakui, Ishige, Fukumoto, Ueda & Ohbayashi, 1984; Miyauchi, Sakui, Ishige, Fukumoto, Ueda, Ito & Ohbayashi, 1984). However, no protoscolex formation has been observed in these domestic ungulates, so three species of voles, ~Iethrianomys rufocaplus bedfordiae, C. rut&s mikado
FIG. 4. Lesions in the lung of naturally infected Norway rat. Periodic acid Schiff stain.
FIG. 5. Fully developed protoscoleces from Wistar rat 7 months after intraperitoneal inoculation with homogenate of E. multilocularis cysts from naturally infected Norway rat.
6-15 pm. The germinal layer was thin, although it showed a reticular structure and calcareous corpuscles, and protoscoleces were observed sporadically (Fig. 3). In the cysts in other organs, the laminated layer and reticular germinal layer were observed, but no protoscolex formation was detected (Fig. 4). In the
and Apodemus arge~te~s, have been considered to be the important intermediate hosts in Hokkaido (Ooi, Inaba & Kamiya, in press). It is doubtful that protoscoleces in the cysts of the present rat could have infected a final host, because they were not completely developed. However, it is assumed that protoscoI~es in this rat could have completed their development in the course of time, because no necrosis was observed and inflammatory cellular reactions were mild. Also, fully developed protoscoleces were recovered from three gerbils and one rat inoculated with homogenate of cysts from this rat. A great many intraspecific variants or strains of Echinococcus have been described from different geographic areas or intermediate host species (Thompson & Lymbery, 1990). Populations of E. mult~Io~u~aris from Europe, Alaska and central North America have been reported to differ in many aspects, including morphology, degree of pathogenicity, developmental characteristics and host specificity (Rausch & Richards, 19’71; Ohbayashi, Rausch & Fay, 1971; Thompson & Eckert, 1983). However, genetic characterization has not been carried out on these populations. Yamashita (1973) assumed that E. multilocularis prevalent in Hokkaido was introduced from St. Lawrence Island, in the Bering Sea, via Komandorskie and Kuril Islands. In a comparative study between the Alaskan and Hokkaido isolates, there were some differences in developmental characteristics in experimentally infected cotton rats, although no difference was detected on biochemical analysis including gel diffusion, GPI isozyme and SDS-PAGE of component proteins (Kawase & Yagi, 1985). The fact that spontaneous E. multilocularis infections in swine have been found frequently in Hokkaido (Sakui et al., f984), as well as the current infection in the rat, may indicate that a different
684
M. OKAMOTO~~~.
population from that in Alaska is prevalent in all or some areas of Hokkaido. In the liver of rats examined, various sized T. taeniaeformis cysts were observed, although it is generally accepted that the rat is completely resistant to reinfection with T. taeniueformis experimentally (Rickard, 1983). Thus, there is a possibility that host factors such as immunosuppression or genetic variation could have contributed to infection with E. multiIocularis in the present case. These points will be further investigated by epidemiological surveys and comparative studies among various isolates, including experimental infection. Although it has been reported that the domestic cat could become a definitive host of E. multilocularis, there has been some dispute as to whether domestic cats play an important role in the parasite’s natural life cycle (Leiby & Kritsky, 1972; Eckert, Miiller & Partidge, 1974; Rausch, 1986; Schwabe, 1986). Vogel (1960) recognized that a cycle involving domestic cats and house mice, Mus musculus, which like the Norway rat, occur in an urban habitat, might exist on farms. In the area of the present survey, the possibility exists for the establishment of an E. multilocularis cycle involving domestic cats and Norway rats. This is because domestic cats have already been shown to act as final hosts (Eckert et al., 1974), and a T. taeniaeformis cycle involving the same hosts already occurs in that area. This cycle is closely related to human activity, so that the risk of infection for humans in such a synanthropic cycle is higher than that in the sylvatic cycle. Acknowledgments-We would like to thank Dr Masashi Ohbayashi, Department of Veterinary Medicine (Parasitology), Rakuno Gakuen University and Dr Robert L. Rausch, Department of Comparative Medicine, School of Medicine, University of Washington for their valuable suggestions. We would also like to thank members of the Department of Veterinary Public Health and Department of Parasitology, Faculty of Veterinary Medicine, Hokkaido University for assistance in collection of the animals and Dr Matthew C. Playford, Department of Parasitology, Faculty of Veterinary Medicine, Hokkaido University for reviewing the manuscript. REFERENCES ECKERTJ., MOLLER B. & PAR~IDGE A. J. 1974. The domestic cat and dog as natural definitive hosts of Echinococcus (Alveococcus) multilocularis in Southern Federal Republic of Germany. Tropical Medicine and Parasitology 2J: 334-337. KAWASES. & YAGI K. 1985. Studies on experimental secondary multilocular hydatidosis. 3. Characterization of Echinococcus mulrilocularis isolated in Abashiri region, north-eastern Hokkaido, Japan. Japanese Journal of Parasitology 32: 81. LEIBY P. D. & KRITSKY D. C. 1972. Echinococcus mulfiloculuris: a possible domestic life cycle in central North America and its public health implications. Journal
ofParasitology%: 1213-1215. LUKASHENKON. P. & ZORIKH~NAV. I. 1961. Epidemiologiia al’veokokkoza (al’veoliarnogo ekhinokokkoza) v tsentral’nykh raionakh Barabinskoi lesostepi Novosibirskoi oblasti. Medical Purasirology (Moscow) 30: 159-168 (in Ohbayashi, 1975). MIYAUCHIT., SAKUI M., ISHIGE M., FUKUMOTOS., UEDA A., ITO M. & OHBAYASHI M. 1984. A case of multilocular echinococcosis in a horse. Japanese Journal of Veterinary Research 32: 171-173. OHBAYASHIM., RAUSCH R. L. & FAY F. H. 1971. On the ecology and distribution of Echinococcus spp. (Cestoda: Taeniidae), and characteristics of their development in the intermediate host. II. Comparative studies on the development of larval E. multilocularis Leuckart, 1863, in the intermediate host. Japanese Journal of Veterinary Research 19, Supplement: l-53. OHBAYASHIM. 1975. Echinococcus. Hokujyukai-shi 19: 126 257 (in Japanese). 001 H. K., INABA C. & KAMIYA M. (in press) Experimental evaluation of mink and Apodemus speciosus in the maintenance of Echinococcus multilocularis life-cycle in Hokkaido, Japan. Journal of Wildlife Diseases. RNJSCH R. L. & RICHARDS S. H. 1971. Observations on parasite-host relationships of Echinococcus multilocularis Leuckart, 1863, in North Dakota. Canadian Journal of Zoology49: 1317-1330. RAUSCH R. L. 1986. Life-cycle patterns and geographic distribution of Echinococcus species. In: The Biology of Echinococcus and Hydatid Disease (Edited by THOMPSON R.C.A.), pp. 44-80. Allen & Unwin, London. RICKARDM. D. 1983. Immunity. In: Biology of the Eucestoda, Vol. 2 (Edited by ARME C. & PAPPAS P.W.), pp. 539-579. Academic Press, London. SAKUI M., ISHIGE M., FUKUMOTOS., UEDA A. & OHBAYASHI M. 1984. Spontaneous Echinococcus multilocularis infection in swine in North-eastern Hokkaido, Japan. Japanese Journal of Parasitology 33: 291-296. SCHWABEC. W. 1986. Current status of Hydatid disease: a zoonosis of increasing importance. In: The Biology of Echinococcus and Hydatid Disease (Edited by THOMPSON R.C.A.), pp. 81-113. Allen & Unwin, London. SMYTH J. D. 1964. The biology of the hydatid organisms. Advances in Parasitology 2: 169-2 19. THOMPSON R. C. A. & ECKERT J. 1983. Observations on Echinococcus multilocularis in the definitive host. Zeitschrift fiir Parasitenkunde 69: 335-345. THOMPSON R. C. A. & LYMBERYA. J. 1990. Echinococcus: biology and strain variation. International Journal for Parasitology 20: 457470. VOGEL V. H. 1960. Tiere als naturliche Wirte des Echinococcus multilocularis in Europa. Zeitschriftfiir Parasitenkunde 11: 3&42. WEBSTERG. A. &CAMERON T. W. M. 1961. Observations on experimental infections with Echinococcus in rodents. Canadian Journal of Zoology 39: 877-891. YABE T. 1979. Eye lens weight as an age indicator in the Norway rat. Journal of the Mammalogical Society of Japan 8: 5455. YAMASHI~A J. 1973. Echinococcus and echinococcosis. In: Progress in Medical Parasitology, Japan 5, pp. 65-123. Meguro Parasitological Museum, Tokyo.
OOZC-7519192 $5.00 + 0.00 Pergamon Press Lrd Q I992 Ausrralim Socieryfor Porosifology
RESEARCHNOTE NATURAL ECHINOCOCCUS MULTILOCULARIS INFECTION IN A NORWAY RAT, RATTUS NORVEGICUS, IN SOUTHERN HOKKAIDO, JAPAN MUNEHIRO OKAMOTO,*~ OSAMU FUJITA,* JIRO ARIKAWA,~ TSUTOMUKUROSAWA,§YUZABURO OKU* and MASAO KAMIYA* *Department
of Parasitology,
§The Institute
of Experimental
Faculty of Veterinary Medicine and $Institute of Immunological Science, Hokkaido University, Sapporo 060, Japan Animal Sciences, Osaka University Medical School, Suita-shi 565, Japan
(Received 23 March 1992; accepted 6 April 1992) AbStraCt~KAMOTO
M., FUJITA O., ARIKAWA J., KUROSAWA T., OKU Y. and KAMIYA M.
1992. Natural
Echinococcus multilocularis infection in a Norway rat, Rattus norvegicus, in southern Hokkaido, Japan. International Journalfor Parasitology 22: 681-684. Forty-two rats, Rattus norvegicus, captured at a garbage dump in southern Hokkaido, Japan, were examined, and one was found to be infected with Echinococcus multilocularis. The lesions were found in the liver, lung, mesenteric lymph nodes, greater omentum and also free in the abdominal cavity. No necrosis was observed in any of the lesions, and inflammatory reactions were mild. Protoscoleces were observed in the large liver cysts. A homogenate of these cysts, when transplanted into the abdominal cavity of three Mongolian gerbils and a rat, yielded numerous fully developed protoscoleces at 4-7 months post-inoculation. Judging from this, it is postulated that the rat could become a natural intermediate host for E. multilocularis in this area. INDEX KEY WORDS: Echinococcus multilocularis; Taenia taeniaeformis; Norway natural infection; intermediate host; protoscolex; Japan.
A wide range of mammals, including rodents, lagomorphs, insectivores and ungulates, have been reported as susceptible to infection with Echinococcus multilocularis eggs @myth, 1964). Arvicoline rodents, mainly of the genera Microtus and Clethrionomys, are the most important in the natural life cycle of E. multilocuZuris, so that in most endemic areas the natural cycle is completed between these rodents and two genera of foxes, Vulpes and Alopex (Rausch,
1986). Domestic dogs and cats are also important as a source of infection for humans, as they capture and eat infected wild voles in some hyperendemic foci such as St. Lawrence Island (Rausch, 1986). However, the source of infection for dogs and cats is more likely to be rats and house mice, because these rodents are commonly captured by such carnivores. Nevertheless, there arc very few reports on natural infection with E. mu/tiloculuris larvae in rats and mice (Ohbayashi, 1975). A natural case of infection in the rat has so far
tPresent address and address for correspondence: The Institute of Experimental Animal Sciences, Osaka University Medical School, Suita-shi 565, Japan.
rat; Rat&s norvegicus;
only been reported once, from Barabinskaya Step, in the Soviet Union, when four of 50 rats examined were infected (Lukashenko & Zorikhina, 1961). In these cases, however, no protoscoleces were observed. As for experimental infection, Webster and Cameron (1961) reported that five rats examined were all negative 16 and 36 weeks after being orally inoculated with E. multilocularis eggs. Thus, it has been considered that rats were resistant to infection with E. multilocularis eggs (Webster & Cameron, 196 I), and do not have an important role to play in the natural cycle of E. multiloculuris. Norway rats were captured alive by traps in October 1989 at a garbage dump in Kamiiso, Southern Hokkaido. Japan. Forty-two rats, with weights ranging from 30 to 305 g, and aged from I to 13 months, estimated from eye lens weight (Yabe, 1979) were examined. Rats were sacrificed under anesthesia, and the helminth parasites in the thoracic and abdominal viscera examined. Nodules and lesions which were difficult to identify were removed from organs and fixed in 10% neutral buffered formahn solution. These tissues were dehydrated in an ethanol series and paraffin sections of 5 pm thickness were made. Sections
682
M. OKAMOTOet al.
FIG. 1. Macroscopic appearance of E. multilocularis lesion in the liver of naturally infected Norway rat (arrow). Two white portions (arrowhead) are the cysts of T. taeniaeformis.
were stained with either hematoxylin+osin or periodic acid Schiff stain for histological examination. Three species of helminths, E. multilocularis (l/42), Taenia taeniaeformis (38/42) and Capillaria hepatica (16/42), were found. The latter two species only parasitized the liver. The infection rate of T. taeniaeformis was very high and the number of these cysts per rat was one to six. The size and developmental stage of T. taeniaeformis were various even in the same rat. Fifteen out of 16 rats infected with C. hepatica were simultaneously infected with T. taeniaeformis. One male rat, with a 305 g body weight and 10.4 months old, was infected with E. multilocularis. This rat was also infected with three cysts of T. taeniaeformis, and with C. hepatica. E. multilocularis lesions were found in the liver, lung, mesenteric lymph nodes, greater omentum and also free in the abdominal cavity. The liver lesions, 15-20 mm in diameter, were multivesicular and macroscopically seemed to be typical cysts of E. multilocularis (Fig. 1). In the largest cyst of this lesion, protoscolex formation was observed. Some of these protoscoleces possessed complete hooks, but suckers were not well defined in any protoscoleces observed (Fig. 2), indicating incomplete development. Many small cystic structures were found in the
FIG. 2. Protoscoleces from the liver lesion of naturally infected Norway rat.
mesenteric lymph nodes, greater omentum and abdominal cavity. In the lung, one lesion, 6 mm in diameter, was observed in the right lobe, and in the left, central and lateral lobes lesions 34 mm in diameter were found. Microscopically, cysts of assorted size, several micrometers to several millimeters, were seen in the liver lesion. In the large cysts, the laminated layer was
Research Note
FIG. 3. Liver lesion in naturally infected Norway rat, showing developing protoscoleces (arrow). Periodic acid Schickstain.
683
adventitial tissue of all cysts, inflammatory cellular reactions were mild despite fibrous proliferations being observed. No necrosis was observed even in the center of the cysts. Three Mongolian gerbils, ~er~o~es unguiculatus, and one Wistar rat, intraperitoneally inoculated with homogenate of E. multilocularis cysts from the naturally infected rat’s liver, were examined at 47 months post-inoculation. All animals were infected and numerous morpholo~cally normal fully developed protoscoleces were observed (Fig. 5). In Hokkaido, spontaneous infection with E. multilocularis has been reported not only from rodents but also pigs and horses (Sakui, Ishige, Fukumoto, Ueda & Ohbayashi, 1984; Miyauchi, Sakui, Ishige, Fukumoto, Ueda, Ito & Ohbayashi, 1984). However, no protoscolex formation has been observed in these domestic ungulates, so three species of voles, ~Iethrianomys rufocaplus bedfordiae, C. rut&s mikado
FIG. 4. Lesions in the lung of naturally infected Norway rat. Periodic acid Schiff stain.
FIG. 5. Fully developed protoscoleces from Wistar rat 7 months after intraperitoneal inoculation with homogenate of E. multilocularis cysts from naturally infected Norway rat.
6-15 pm. The germinal layer was thin, although it showed a reticular structure and calcareous corpuscles, and protoscoleces were observed sporadically (Fig. 3). In the cysts in other organs, the laminated layer and reticular germinal layer were observed, but no protoscolex formation was detected (Fig. 4). In the
and Apodemus arge~te~s, have been considered to be the important intermediate hosts in Hokkaido (Ooi, Inaba & Kamiya, in press). It is doubtful that protoscoleces in the cysts of the present rat could have infected a final host, because they were not completely developed. However, it is assumed that protoscoI~es in this rat could have completed their development in the course of time, because no necrosis was observed and inflammatory cellular reactions were mild. Also, fully developed protoscoleces were recovered from three gerbils and one rat inoculated with homogenate of cysts from this rat. A great many intraspecific variants or strains of Echinococcus have been described from different geographic areas or intermediate host species (Thompson & Lymbery, 1990). Populations of E. mult~Io~u~aris from Europe, Alaska and central North America have been reported to differ in many aspects, including morphology, degree of pathogenicity, developmental characteristics and host specificity (Rausch & Richards, 19’71; Ohbayashi, Rausch & Fay, 1971; Thompson & Eckert, 1983). However, genetic characterization has not been carried out on these populations. Yamashita (1973) assumed that E. multilocularis prevalent in Hokkaido was introduced from St. Lawrence Island, in the Bering Sea, via Komandorskie and Kuril Islands. In a comparative study between the Alaskan and Hokkaido isolates, there were some differences in developmental characteristics in experimentally infected cotton rats, although no difference was detected on biochemical analysis including gel diffusion, GPI isozyme and SDS-PAGE of component proteins (Kawase & Yagi, 1985). The fact that spontaneous E. multilocularis infections in swine have been found frequently in Hokkaido (Sakui et al., f984), as well as the current infection in the rat, may indicate that a different
684
M. OKAMOTO~~~.
population from that in Alaska is prevalent in all or some areas of Hokkaido. In the liver of rats examined, various sized T. taeniaeformis cysts were observed, although it is generally accepted that the rat is completely resistant to reinfection with T. taeniueformis experimentally (Rickard, 1983). Thus, there is a possibility that host factors such as immunosuppression or genetic variation could have contributed to infection with E. multiIocularis in the present case. These points will be further investigated by epidemiological surveys and comparative studies among various isolates, including experimental infection. Although it has been reported that the domestic cat could become a definitive host of E. multilocularis, there has been some dispute as to whether domestic cats play an important role in the parasite’s natural life cycle (Leiby & Kritsky, 1972; Eckert, Miiller & Partidge, 1974; Rausch, 1986; Schwabe, 1986). Vogel (1960) recognized that a cycle involving domestic cats and house mice, Mus musculus, which like the Norway rat, occur in an urban habitat, might exist on farms. In the area of the present survey, the possibility exists for the establishment of an E. multilocularis cycle involving domestic cats and Norway rats. This is because domestic cats have already been shown to act as final hosts (Eckert et al., 1974), and a T. taeniaeformis cycle involving the same hosts already occurs in that area. This cycle is closely related to human activity, so that the risk of infection for humans in such a synanthropic cycle is higher than that in the sylvatic cycle. Acknowledgments-We would like to thank Dr Masashi Ohbayashi, Department of Veterinary Medicine (Parasitology), Rakuno Gakuen University and Dr Robert L. Rausch, Department of Comparative Medicine, School of Medicine, University of Washington for their valuable suggestions. We would also like to thank members of the Department of Veterinary Public Health and Department of Parasitology, Faculty of Veterinary Medicine, Hokkaido University for assistance in collection of the animals and Dr Matthew C. Playford, Department of Parasitology, Faculty of Veterinary Medicine, Hokkaido University for reviewing the manuscript. REFERENCES ECKERTJ., MOLLER B. & PAR~IDGE A. J. 1974. The domestic cat and dog as natural definitive hosts of Echinococcus (Alveococcus) multilocularis in Southern Federal Republic of Germany. Tropical Medicine and Parasitology 2J: 334-337. KAWASES. & YAGI K. 1985. Studies on experimental secondary multilocular hydatidosis. 3. Characterization of Echinococcus mulrilocularis isolated in Abashiri region, north-eastern Hokkaido, Japan. Japanese Journal of Parasitology 32: 81. LEIBY P. D. & KRITSKY D. C. 1972. Echinococcus mulfiloculuris: a possible domestic life cycle in central North America and its public health implications. Journal
ofParasitology%: 1213-1215. LUKASHENKON. P. & ZORIKH~NAV. I. 1961. Epidemiologiia al’veokokkoza (al’veoliarnogo ekhinokokkoza) v tsentral’nykh raionakh Barabinskoi lesostepi Novosibirskoi oblasti. Medical Purasirology (Moscow) 30: 159-168 (in Ohbayashi, 1975). MIYAUCHIT., SAKUI M., ISHIGE M., FUKUMOTOS., UEDA A., ITO M. & OHBAYASHI M. 1984. A case of multilocular echinococcosis in a horse. Japanese Journal of Veterinary Research 32: 171-173. OHBAYASHIM., RAUSCH R. L. & FAY F. H. 1971. On the ecology and distribution of Echinococcus spp. (Cestoda: Taeniidae), and characteristics of their development in the intermediate host. II. Comparative studies on the development of larval E. multilocularis Leuckart, 1863, in the intermediate host. Japanese Journal of Veterinary Research 19, Supplement: l-53. OHBAYASHIM. 1975. Echinococcus. Hokujyukai-shi 19: 126 257 (in Japanese). 001 H. K., INABA C. & KAMIYA M. (in press) Experimental evaluation of mink and Apodemus speciosus in the maintenance of Echinococcus multilocularis life-cycle in Hokkaido, Japan. Journal of Wildlife Diseases. RNJSCH R. L. & RICHARDS S. H. 1971. Observations on parasite-host relationships of Echinococcus multilocularis Leuckart, 1863, in North Dakota. Canadian Journal of Zoology49: 1317-1330. RAUSCH R. L. 1986. Life-cycle patterns and geographic distribution of Echinococcus species. In: The Biology of Echinococcus and Hydatid Disease (Edited by THOMPSON R.C.A.), pp. 44-80. Allen & Unwin, London. RICKARDM. D. 1983. Immunity. In: Biology of the Eucestoda, Vol. 2 (Edited by ARME C. & PAPPAS P.W.), pp. 539-579. Academic Press, London. SAKUI M., ISHIGE M., FUKUMOTOS., UEDA A. & OHBAYASHI M. 1984. Spontaneous Echinococcus multilocularis infection in swine in North-eastern Hokkaido, Japan. Japanese Journal of Parasitology 33: 291-296. SCHWABEC. W. 1986. Current status of Hydatid disease: a zoonosis of increasing importance. In: The Biology of Echinococcus and Hydatid Disease (Edited by THOMPSON R.C.A.), pp. 81-113. Allen & Unwin, London. SMYTH J. D. 1964. The biology of the hydatid organisms. Advances in Parasitology 2: 169-2 19. THOMPSON R. C. A. & ECKERT J. 1983. Observations on Echinococcus multilocularis in the definitive host. Zeitschrift fiir Parasitenkunde 69: 335-345. THOMPSON R. C. A. & LYMBERYA. J. 1990. Echinococcus: biology and strain variation. International Journal for Parasitology 20: 457470. VOGEL V. H. 1960. Tiere als naturliche Wirte des Echinococcus multilocularis in Europa. Zeitschriftfiir Parasitenkunde 11: 3&42. WEBSTERG. A. &CAMERON T. W. M. 1961. Observations on experimental infections with Echinococcus in rodents. Canadian Journal of Zoology 39: 877-891. YABE T. 1979. Eye lens weight as an age indicator in the Norway rat. Journal of the Mammalogical Society of Japan 8: 5455. YAMASHI~A J. 1973. Echinococcus and echinococcosis. In: Progress in Medical Parasitology, Japan 5, pp. 65-123. Meguro Parasitological Museum, Tokyo.