Reproductive potential of Echinococcus multilocularis in experimentally infected foxes, dogs, raccoon dogs and cats

Abstract

A total of 15 red foxes, 15 raccoon dogs, 15 domestic dogs and 15 domestic cats were each infected with 20,000 protoscolices of Echinococcus multilocularis. At 35, 63, and 90 days post inoculation (dpi), five animals from each group were necropsied and the worm burdens determined. The highest worm burdens in foxes (mean of 16,792) and raccoon dogs (mean of 7930) were found at 35 dpi. These declined to a mean of just 331 worms in foxes and 3213 worms in raccoon dogs by day 63 with a further decline to 134 worms in foxes and 67 worms in raccoon dogs by day 90. In dogs, there was no significant difference between worm burdens recovered at days 35 (mean of 2466) and day 90 (mean of 1563), although reduced numbers were recovered on day 63 (mean of 899). In cats, worms were found in four animals 35 dpi (mean of 642), in three at 63 dpi (mean of 28) and in two at 90 dpi (mean of 57). Faecal egg counts were determined at 3 day intervals from 25 dpi. A mathematical model of egg excretion dynamics suggested that the mean biotic potential per infected animal was high in foxes (346,473 eggs); raccoon dogs (335,361 eggs) and dogs (279,910 eggs) but very low for cats (573 eggs). It also indicated that approximately 114, 42 and 27 eggs per worm were excreted in the faeces of dogs, raccoon dogs and foxes, respectively. The fecundity of worms in cats was low with an average of less than one egg per worm. The peak levels of coproantigen were detected earlier in foxes and raccoon dogs than in dogs. Eggs recovered from foxes, raccoon dogs and dogs resulted in massive infections in experimental mice. However, metacestodes did not develop from eggs originating from infected cats. It is concluded that foxes, raccoon dogs and dogs are good hosts of E. multilocularis. In contrast, the low worm establishment, the very few excreted eggs and the lack of infectivity of eggs strongly indicate that cats play an insignificant role in parasite transmission.

Introduction

The life-cycle of Echinococcus multilocular predominantly involves foxes (Vulpes vulpes in temperate regions and Alopex lagopus in arctic and sub-arctic regions) as definitive hosts and many species of rodents can act as intermediate hosts (Schantz et al., 1995). Foxes are thought to be the main sources of environmental contamination with eggs of E. multilocularis in most endemic areas (Eckert and Deplazes, 2004), but infections have also been found in coyotes (Canis latrans), raccoon-dogs (Nyctereutes procyonoides), wolves (Canis lupus) and occasionally wild cats (Felis libyca) (Vuitton et al., 2003). However, it is not known if any other species can maintain the E. multilocularis cycle independently from the fox reservoir.

In certain areas, a relatively high prevalence of E. multilocularis has been found in domestic dogs (1–12%). These include endemic foci in Alaska, China and Central Europe (Schantz et al., 1995, Deplazes et al., 2004, Budke et al., 2005). In the past, many such studies could only be based on necropsy results, with the disadvantage that the animals examined represented a selected population. More recent studies from China were based on the use of arecoline purgation (Budke et al., 2005) but have the disadvantage of the undefined diagnostic sensitivity of this technique. Using a coproantigen-ELISA in combination with a confirmatory PCR for ELISA positive results, larger numbers of dogs have recently been investigated in Europe. Deplazes et al. (1999) recorded a prevalence of 0.3% (95% confidence interval (CI) 0.04–1.09%) whilst Gottstein et al. (2001) found up to 6.9% (95% CI 2.60–14.57%) in Swiss dog populations. Although dogs may not maintain a synanthropic cycle of E. multilocularis in Europe, even a low prevalence may constitute a zoonotic risk due to their proximity to humans (Kern et al., 2004).

Prevalence of E. multilocularis in cat populations, as determined at necropsy, ranged between 0.5 and 3.7% in various endemic areas (Eckert and Deplazes, 2004) but generally only low worm burdens and variable development of the proglottids have been detected. Although small numbers of E. multilocularis eggs from faeces of naturally infected cats have been characterized by PCR (Deplazes et al., 1999, Gottstein et al., 2001), the infectivity of such eggs have never been proven.

The raccoon dog (N. procyonoides) originated in Eastern Asia and was introduced as a game and farm animal into the Baltic part of the former Soviet Union in the period 1930–1955 and has gradually spread to Western Europe along the Baltic Sea coast (Prûsaitè et al., 1988, Asikainen et al., 2003). First reports of E. multilocularis infection in raccoon dogs were from Japan and recently Thiess et al. (2001) found E. multilocularis infection in raccoon dogs in Germany. In a recent study in Japan, three of 15 (23%) raccoon dogs were found to be infected with an average of 505 worms (Yimam et al., 2002). Thus, only very limited information about parasite numbers and development is available and the epidemiological significance of the raccoon dog as a definitive host of E. multilocularis is unknown. Because of the establishment of this carnivore in new areas of Europe, such information is of public health significance.

In this study, the dynamics of E. multilocularis worm burden, excretion of eggs and coproantigens were compared in experimentally infected foxes, raccoon dogs, dogs and cats.