The epidemiological status of Echinococcus multilocularis in animals in Hokkaido, Japan

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1 Mammal Study 30: S101 S105 (2005) the Mammalogical Society of Japan The epidemiological status of Echinococcus multilocularis in animals in Hokkaido, Japan Kenichi Takahashi *, Kohji Uraguchi and Shinichi Kudo Department of Biological Science, Hokkaido Institute of Public Health, N-19 W-12, Kita-ku, Sapporo , Japan Abstract. Hokkaido is the northernmost island and the only endemic area of alveolar echinococcosis caused by Echinococcus multilocularis in Japan. The first human case was reported in After the discovery of this disease, various epidemiological surveys have been conducted on Echinococcus multilocularis in animals. Accumulated longitudinal epidemiological data clearly showed the geographic changes of endemic areas in Hokkaido during the last 70 years. The expansion of the endemic area and the increase of the prevalence of the parasite in foxes have increased the risk of infection for residents in this region during the last two decades. This paper reviews the epidemiological situation and control options of this parasite in animals after a brief description on the historical background of this disease in Hokkaido. Key words: animal host, control, E. multilocularis, epidemiology, Japan. Alveolar echinococcosis caused by the metacestode stage of E. multilocularis is one of the serious zoonoses found in the Northern Hemisphere (Schanz et al. 1995). In Japan, Hokkaido is the only endemic area of this parasitic disease. Since an outbreak of alveolar echinococcosis on Rebun Island, various field surveys have been conducted on Echinococcus multilocularis in animals (Yamashita 1978; Takahashi et al. 1999). Red foxes, Vulpes vulpes, are the main definitive hosts and voles, especially the gray-sided vole, Clethrionomys rufocanus, are the important intermediate hosts in this region. Further, some sporadic infection of dogs and cats has been reported as definitive hosts. After 1983, when the expansion of the endemic areas was confirmed, extensive epidemiological surveys of E. multilocularis prevalence in animals were carried out all over Hokkaido. These surveys showed a spread of the parasite in the 1980s and an increase in the infection rates of foxes in the 1990s. These results have been compiled by the Hokkaido Echinococcosis Control Council, and have been used by municipal governments in newly identifies endemic areas as basic data for the implementation of health examinations and health education programs. Appropriate management of the dog and fox population as sources for human infection is crucial. Brief description on the historical background of alveolar echinococcosis in Hokkaido Up to 2003, more than 460 cases of human alveolar echinococcosis have been reported on Hokkaido. The first case of alveolar echinococcosis was reported in Hokkaido in 1937 (Tsunoda et al. 1937). The patient had lived in Rebun Island, with an area of 83 km 2, 45 km from the main island of Hokkaido. Twelve pairs of red foxes were introduced to the island from Simushir Island, Middle Kuril and were released to control of the number of voles as well as for the production of fox fur during the year of 1924 and It is believed that infected foxes were transferred and the life cycle of this parasite was established among animals on this small Island (Yamashita 1973). Up to the present, 131 human cases have been recorded in this small Island. However, the control of this disease had so far been successful and there have been no recent outbreaks of the disease on this Island. Another endemic area was found in 1965 with the diagnosis of human cases among the residents of the Nemuro district, in the eastern part of Hokkaido (Yamashita 1978). Epidemiological surveys showed the endemic area of 10 municipalities in the Nemuro and Kushiro districts, and still new human cases have *To whom correspondence should be addressed. takaken@iph.pref.hokkaido.jp

2 S102 Mammal Study 30 (2005) been reported. Since 1983, some human cases have been reported in other areas of Hokkaido according to the extension of the endemic area (Kimura et al. 1999). Animal host and prevalence Definitive host The main definitive host in the natural environment is the red fox. From 1966 to 2003, a total of 23,852 foxes were dissected in Hokkaido, and of these, 4,561 (19.1%) were confirmed to be infected with E. multilocularis (Hokkaido Prefecture Government 2004). However, recent data (39.7% of 1972 foxes during 1999 and 2003) shows the increase of E. multilocularis in foxes (Table 1, Hokkaido Prefecture Government 2000, 2001, 2002, 2003, 2004). Dogs are also important definitive hosts because of their potential to become infection sources for humans. According to epidemiological surveys conducted so far ( ), E. multilocularis was found in 1.0% of 9,907 dogs examined (Hokkaido Prefecture Government 2004). These survey results on dogs reveal the importance of properly managing domestic dogs to prevent them from eating field rodents. The first case of adult E. multilocularis infection in a cat was found on Rebun Island (Ambo et al. 1954). Thereafter, between 1966 and 1996, 91 cats were examined during in Hokkaido, and five (5.5%) were infected with the parasite (Hokkaido Prefecture Government 1997). Further, 1.1% of 92 raccoon dogs were infected with adult E. multilocularis (Hokkaido Prefecture Government 2004). A further study showed that three more cases of E. multilocularis infection in raccoon dogs were found in Hokkaido (Yimam et al. 2002). Intermediate host Six species belonging to Muridae have been found to be infected with larval stage of E. multilocularis. Table 1. Prevalence of adult Echinococcus multilocularis in red foxes in Hokkaido from 1999 to Year No. of exam. No. of posi. (%) (45.8) (38.5) (39.0) (31.6) (43.1) Total (39.7) Of these, three species of the genus Clethrionomys (C. rufocanus, C. rutilus and C. rex) have been confirmed as suitable intermediate hosts of E. multilocularis (Yorozuya et al. 1968; Hasegawa 1970; Takahashi and Nakata 1995). In particular, the gray-sided vole plays a crucial role in maintaining the life cycle of E. multilocularis because of its wide distribution on grasslands throughout the prefecture, it is also the main prey of the fox and the presence of numerous mature protoscolices in the cysts of this species (Abe 1975; Kondo et al. 1986; Takahashi and Uraguchi 1996). Among species that belong to the subfamily Murinae, Apodemus argenteus, Mus musculus and Rattus norvegicus were confirmed as intermediate hosts of E. multilocularis (Yagi et al. 1984; Takahashi et al. 1986; Iwaki et al. 1992; Okamoto et al. 1992). However, there have only been a few cases detected and it is not clear what their role is in the transmission of the parasite in this region. Further, E. multilocularis was also detected in one of Sorex caecutiens and three of S. unguiculatus captured in Nemuro City (Takahashi and Uraguchi 1994). Larval stage of E. multilocularis have been detected in pigs (order Artiodactyla) and horses (order Perissodactyla), in meat inspection centers in Hokkaido (Miyauchi et al. 1984; Sakui et al. 1984). These were the first records of E. multilocularis infection in pigs and horses in Japan. In these two species of domestic ungulates, however, protoscolex formation in the cysts has not been observed, and they play no part in the maintenance of the life cycle of E. multilocularis. Sporadical E. multilocularis infection among zoo animals belonging to various zoos have been reported (Ohbayashi 1996). So far, larval stages of E. multilocularis were found in orangutans (Pongo Pygmaeus), Japanese macaques (Macaca fuscata), gorillas (Gorilla gorilla) and ringtailed lemurs (Lemur catta). Changes of endemic areas Endemic areas before 1970s Various epidemiological surveys had been conducted on Rebun Island. However, E. multilocularis were detected only two cats and two dogs, and the detection of worms in intermediate hosts other than humans has never been recorded (Yamashita 1978). Until the mid 1960s, the distribution of E. multilocularis was not confirmed in any other area in Hokkaido. In 1965, two human cases were diagnosed in Nemuro City, Eastern Hokkaido, and a new endemic area of E.

3 Takahashi et al., E. multilocularis in animals in Japan multilocularis was found in the eastern part of the prefecture. Field examinations were conducted on animal hosts in this region from 1966 to 1971, worms were detected in foxes and dogs (definitive hosts) and two species of voles, Clethrionomys rutilus and C. rufocanus (intermediate hosts), collected from the 10 municipalities. In these and surrounding municipalities, field surveys were continually carried out on foxes and dogs, and no new E. multilocularis endemic areas were found outside Rebun Island (town) and 10 municipalities in the Numuro and Kushiro district (total 11 municipalities) until Expansion of E. multilocularis distribution In , E. multilocularis infection of domestic pigs was confirmed in the Abashiri Meat Inspection Center. The area in which these pigs were raised was outside the known endemic areas. Then prefecture-wide epidemiological surveys regarding animals were carried out to identify the geographic range of the parasite. These surveys led to the detection of the parasite in various species of animal hosts collected from 26 new endemic municipalities by April Subsequently, the number of confirmed E. multilocularis endemic municipalities added to the list every year rose to 103 in April 1987, 158 in April 1990, and 189 in April The April 1993 figure shows that the known E. multilocularis distribution area has spread to most parts of the prefecture. Furthermore, the E. multilocularis infection rates of foxes showed a drastic increase for all 14 administrative districts in Hokkaido from 1985 to Between 1985 and 1987, the rates of infection in foxes exceeded 30% in only two districts (the Nemuro district in eastern Hokkaido and the Oshima district in southern Hokkaido). Subsequently, infection rates in other areas exhibited upward trends, with the number of districts recording an infection rate of over 30% rising to 10 in the period and 12 in the , respectively. The longitudinal epidemiological surveys of E. multilocularis infection in animals revealed a spread of E. multilocularis in the 1980s and increase of infection rates in the 1990s in Hokkaido. Options for the prevention of human infection from definitive hosts Epidemiological surveys show the appropriate management of red fox and dog populations is key to reduce S103 the infection risk for humans in this region. According to epidemiological surveys conducted so far, the infection rate among dogs is considerably lower than in foxes. Further, the potential role of dogs in a cycle of transmission in this region is considered to be limited because of the limited number of stray dogs controlled by the dog registration system (Takahashi and Mori 2001). However, contact between humans and domestic dogs occurs much more frequently than contact between humans and foxes. The proper handling of domestic dogs in order to prevent them from eating field rodents and the treatment of pet dogs with deworming drugs as needed are applicable effective countermeasures to reduce the human infection risk from dogs. Moreover, such dog management measures are crucial so as not to allow the spread of the parasite into the outside area of Hokkaido by transfer of the infected dogs that originated in this region. The red fox is the principal definitive host for the maintenance of the E. multilocularis cycle in this region. Recent years, some preliminary attempts to reduce the parasite biomass with deworming drugs have been conducted. Following the pioneer approach of fox baiting with prasiquantel in Germany (Shelling et al. 1997), small scale trials to evaluate the efficacy of fox chemotherapy were carried out in Hokkaido. Prasiquantel tablets in fish sausage were placed near fox dens every month for 13 months in a 90 km 2 area of Koshimizu town, eastern Hokkaido (Tsukada et al. 2002). It was shown that coproantigen ELISA positive rate decreased from 60% to 30%. Another control trial of E. multilocularis in foxes has been conducted in the Nemuro peninsula (135 km 2 ). Commercially available baits (containing 50 mg praziquantel) were distributed in densities of 15 per km 2 along roadsides on the peninsula outside towns and villages. Baits were distributed 17 times from Nov to Jan. 2004, and the prevalence of E. multilocularis in foxes by necropsy decreased from 67% to 23% within this period (Takahashi et al. 2002, 2004). There were several similar approaches of fox chemotherapy in Europe. These results showed the efficacy in the decrease of fox infection rate, though eradication was never achieved (Deplazes and Hegllin 2004). Appropriate selection of target areas for anthelmintic treatment of foxes is crucial for the effective prevention of human infection with decreasing parasite biomass.

4 S104 Mammal Study 30 (2005) Acknowledgment: We are grateful to Drs. H. Honma, Y. Sawada, and M. Yonekawa of Hokkaido Institute of Public Health for their encouragement of this publication. Further, we would like to give our acknowledgement to the staffs of Food Sanitation Division, Department of Health and Welfare, Hokkaido Prefecture Government for their support of our research activity. References Abe, H Winter food of the red fox, Vulpes vulpes schrencki Kishida (Carnivore: Canidae), in Hokkaido, with special reference to vole populations. Applied Entomology and Zoology 10: Ambo, H., Ichikawa, K., Iida, H. and Abe, N On echinococcosis alveolaris, endemic parasitosis in Rebun Island. Special Report of Hokkaido Institute of Public Health 4: 1 19 (in Japanese). Deplazes, P. and Hegglin, D Control of Echinococcus multilocularis in definitive host populations. In (P. Torgerson and B. Shaikenov, eds.) Echinococcosis in Central Asia: Problems and Solutions. Pp Almaty, Dauir, Zurich. 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