ISRAEL JOURNAL OF
VETERINARY MEDICINE
VOLUME
55 (2) 2000
ECHINOCOCCOSIS MULTILOCULAR AND ALVEOLAR HYDATID DISEASE IN HOKKAIDO
JAPAN
1
2
2
2
2
M. Furth , M. Kamiya , H. Sakai , N. Nonak , Y. Oku andJ.El-On3
1. Veterinary Services and Animal Health, Ministry of Agriculture, Hadera Veterinary District
Office
2. Graduate School of Veterinary Medicine, Hokkaido University, Sapporo, Japan.
3. Department of Microbiology and Immunology, Faculty of Health Science,
Ben-Gurion University of the Negev, Beer-Sheva
Summary
In this short review of Echinococcus multilocularis in the island of Hokkaido, we describe the
life cycle and epidemiology of the parasite and how it was introduced to Hokkaido by a single
infected red fox from Russia in 1924. Since then, it has spread all over the island and from the
end of 1997, 373 persons had undergone surgery, and from 5 to 20 new patients are
confirmed each year. A comprehensive control program to reduce or eliminate the source of
infection is based on deworming of red foxes by giving praziquantle, coupled with monitoring
of the dynamics of infection through coproantigen detection (sELISA). Public education aimed
at prevention of feeding and taming wild foxes by humans is an integral part of the program.
Introduction
Hokkaido is located at the northern end of the Japan Islands. It has an area of 83,450 sq. km
or 22% of the total land area of Japan with 5,960,000 inhabitants.
Hokkaido is the most productive food source in Japan. It consists of one large and five
smaller islands (Rebun is one of them). Multilocular echinococcosis, caused by the larval
stage of Echinococcus multilocular, is an important zoonosis with a high mortality rate. In
Hokkaido the prevalence among inhabitants has been very low although parasites are rapidly
becoming more prevalent in recent years. The larval stage develops within the liver and lungs
of infected human patients while growth of the slow or rapid invasive pseudomaligene causes
mortality.
Life cycle and
epidemiology of
E. multilocularis
The natural
definitive host is
the wild canid,
fox and small
mammal, and the
intermediate
hosts are mainly
arvicolid and
cricetid rodents
(Fig. 1). The
adult stage, the
strobila, occurs in
the intestine of
foxes, genus
vulpes and
Aloper, as well as
in dogs, coyotes
and wolves.
Kamiya et al.
found that cats
could also serve
as a definite host
(1). The natural
cycle is
completed
through the
predator-prey
relationship.
The prevalence of cestodes in the fox intestine is highest during the autumn following several
months of feeding on Voles mirocrotus. In winter, accumulating snow prevents efficient
hunting of voles and foxes must utilize other food sources. The fox expels the cestodes during
winter (2). E. multilocularis is limited to the northern regions of the world: Europe, Eastern
Russia, Alaska, Canada, Hokkaido, but was recently found also in India, Middle East
(Turkey), Iran, Tunsia and North Africa. In contrast to E. granulosus, the cestode has very
limited genetic variation; E. multilocularis isolates from Germany, Japan, Alaska have
identical nucleotide sequences (3).
Human prevalence in Hokkaido
The first patient with echinococcosis living on Rebun Island was discovered in 1937 at
Otaru, 134 patients have been identified as Rebun cases till 1989. The first Kion-sen cases
were found in 1968 and 208 patients have been treated until 1979. Since then human cases
occur sporadically throughout Hokkaido (4). By the end of 1997, 373 persons had undergone
surgery, and 5 to 20 new patients are confirmed each year. In addition about 400 persons
each year in Hokkaido are provisionally diagnosed as being infected by imaging and serology
(5). Although the prevalence among inhabitants is very low, infestation is rapidly spreading in
recent years (Fig 2).
Sato et al, (6) investigated responsiveness to treatment and prognosis of the disease with
historical comparison of screening systems. The patients were classified in three groups;
group A detected by current screening system of enzyme-linked immunosorbent assay and
ultrasound since 1984; group B detected by serological screening performed between 1974
and 1984 and group C, non-screened patients diagnosed accidentally. Early lesions are found
most frequently in group A. The five years survival rate was 100% in group A, 74% in B and
69% in C, with a significant intergroup difference. The current system favours early diagnosis
of the disease, contributing to its responsiveness to treatment and to better prognosis.
Nagno et al, (7) investigated the prevalence of human alveolar echinocococcosis in
Hokkaido by western blot analysis capable of classifying persons infected with E.
multilocularis into two groups: the "complete type" that showed multiple bands of various
molecular weights and the incomplete types with a few bands of low molecular weight. From
the geographic distribution, those with the complete type first appeared in 1992 in Western
Hokkaido. The age distribution indicates that the complete type pattern has increased since
1990 in less than 30 years old.
Prevalence and diagnostic methods for foxes and vulpes infected with E. multilocularis
in Hokkaido
E. multilocularis is believed to have been introduced into Rebun Island by infected red
foxes translocated from the middle Kuriles (Russia) during 1924 and 1926. Kamiya and
Obayashi found 328 infected red foxes diagnosed at necropsy in the Namura and Kashiro
districts of Hokkaido during 1966 to 1973 (8). The distribution tendency of the patients
coincides with the explosion of the infection of red foxes with Echinococcus multilocularis in
Hokkaido after 1980. In 1985 Kamiya found 10% of foxes infected at necropsy. This
increased to 20% in 1992, 39.5% in 1993 and 36.2% in 1997.
Detection methods: Coproantigen ELISA performed on fecal samples showed positive
results in 38/40 (95%) and 95/97 (97.9%) in 1990 and 1992, respectively. The results suggest
that detection of coproantigen is useful in field surveys of naturally infected foxes (9).
E. multilocularis coproantigens detection was applied for monitoring the parasite in families
of foxes. The results showed that cubbing dens are one of the important endemic foci where
intermediate hosts frequently ingest eggs derived from cub feces. Fox breeding dens were
found around urban areas. Out of 21 dens in urban areas 13 were coproantigen positive while
taenid egg positive feces were also found. These results suggest that the life cycle of E.
multilocularis be probably maintained even in the urban area of Sapporo City (10).
Prevalence in rodents
During May through October 1983, rodents and shrews were caught in Asahikawa and
Kushiro districts and examined for echinococcal infection. Of 603 animals examined in Kusiro
district, one was positive but no evidence was found in animals from Asahikawa (11) (Fig. 3).
In 1992 of 42 rats captured at garbage dumps in southern Hokkaido, one was infected (12).
Strategy for controlling E.multilocularis in Hokkaido
The distribution of the patients coincided with the explosion of E. multilocularis in foxes in Hokkaido
after 1980 (10). The control programs having invariably been aimed to reduce or eliminate the
infection in humans. The designed outcome is a satisfactory decrease in prevalence of human cases.
A comprehensive control program was started in Hokkaido in 1997. This included deworming of red
foxes by administration of praziquantel to foxes in the wild and monitoring its progress with a
coproantigen sandwich ELISA performed on fecal samples. A massive education campaign aimed at
the population consisted of prevention of feeding or taming red foxes and washing all agricultural
products. The coming decades will tell whether the campaign has achieved its goal (13,14).
References
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