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The Fox (Vulpes Vulpes) As a Reservoir for Canine Angiostrongylosis in Denmark Field Survey and Experimental Infections

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The Fox (Vulpes Vulpes) As a Reservoir for Canine Angiostrongylosis in Denmark Field Survey and Experimental Infections Acta vet. scand. 1992,33, 357-362. The Fox (Vulpes vulpes) as a Reservoir for Canine Angiostrongylosis in Denmark Field survey and experimental infections By G. Bolt, J. Monrad, P. Henriksen, H. H. Dietz, J. Koch, E. Bindseil and A. L. Jensen Royal Veterinary and Agricultural University, Frederiksberg, and National Veterinary Laboratory, Arhus , Denmark. Bolt, G., J. Monrad, P. Henriksen, H. H. Dietz, J. Koch, E. Bindseil and A. L. Jensen: The fox (Vulpes vulpes) as a reservoir for canine angiostrongylosis in Denmark. Acta vet. scand, 1992, 33, 357·362. - Until recently, Angiostrongylus vasorum was not con­ sidered to be an endogenous Danish parasite, since demonstration of this worm had been confined to necropsy findings in 2 dogs, both of which had visited France. During the last 2 years, however, clinical cases have been diagnosed among a conside­ rable number of Danish dogs, none of which had ever been outside Denmark. All these cases have occurred north of Copenhagen, where an endemic focus seems to exist. In this field survey A. vasorum was found for the first time in wild Danish red foxes. Furthermore, experimental infections showed that the parasite can be transfer­ red between foxes and dogs. Consequently, the wild fox population must be conside­ red a potential reservoir for transfer of A. vasorum to domestic dogs. Angiostrongylus vasorum; experimental transfer. Introduetlon Angiostrongylus vasorum (French heart­ diagnosis is based on the demonstration of worm) is a metastrongyloid parasite of the the characteristic first stage larvae (Ll) in domestic dog (Canis familiaris) and other faecal samples analyzed by the Baermann carnivores belonging to Canidae. The adult method (Jacobs & Prole 1975, Iergensen & worms parasitize in the right atrium of the Madsen 1982). heart and particularly in the pulmonary In Europe A. vasorum is known to be arteries. The life cycle is indirect with a num­ endemic among dogs in south-west France ber of mollusc species acting as obligatory (Dorchies 1976, Guilhon & Cens 1973), Ire­ intermediate hosts (Guilhon 1965, Guilhon land (Dodd 1973, Jacobs & Prole 1975), and 1967, Guilhon & Cens 1973,). The pathologi­ in south-west England (Jones et al. 1980, cal and clinical manifestations of canine Simpson & Neal 1982). Sporadic cases have angiostrongylosis are multiple, as reported been reported from other parts of France elsewhere (Dodd 1973, Guelfi 1976, Prest (Guilhon 1969), south-east England (Cobb & wood et al. 1981, Schelling et al. 1986). The Fisher 1990), former West Germany (Pal major symptoms are respiratory distress and laske 1967), Spain (Sanchez et al. 1979), Swit­ loss of condition (Cobb & Fisher 1990, Guelfi zerland (Eckert & Ldmmler 1972, Neff1971), 1976, Koch & Bolt 1990). The parasitological and from the European part of the former Acta vet. scand. vol. 33 no. 4 - 1992 358 G. Bolt et al. Sovjet Union (Eckert & Liimmler 1972, ate vicinity of humans and their dogs. The Rosen et al. 1970). Outside Europe the para­ present study was designed to examine the site has been reported to be endemic among occurrence of A. vasorum in the red fox pop­ dogs in Uganda iBwangamoi 1972), and spo­ ulation in the locality north of Copenhagen, radic cases have been reported from dogs in where the canine outbreaks had occurred. Brasil (Lima et al. 1985, Rosen et al. 1970), Furthermore, artificial infections were estab­ Columbia (Rosen et al. 1970), the United lished in order to investigate, whether strains States (Williams 1985), and from the Asiatic of A. vasorum isolated from Danish foxes part of the former Sovjet Union (Eckert & and dogs might be transmissible to dogs and Liimmler 1972). All cases reported from the foxes, respectively. United States have occurred among import­ ed dogs. Materials and methods Among foxes (Vulpes vulpes) A. vasorum Examination ofwild foxes has been reported from France (Guilhon During the period October 1990 to May 1991 1971), Ireland (Guilhon 1971), Italy (Poli et a total of 15 adult red foxes (V. vulpes) from al. 1985), Spain tTarazona 1974), the former the above mentioned region were examined Sovjet Union (Eckert & Liimmler 1972, for A. vasorum. Of these 13 foxes were killed Rosen et al. 1970), Germany (Rosen et al. during hunting and can therefore be consid­ 1970) and Canada (Smith & ThrelfallI973). ered fairly representative of the fox popula­ In Italy and France the fox is considered to tion at the hunting ground, which is located be a reservoir for transmission of A. vasorum in the northern outskirts of Copenhagen to domestic dogs (Guilhon 1965, Guilhon (Jregersborg Game Reserve). Faecal samples 1971, Poli et al. 1985). Guilhon succesfully from all 15 foxes were subjected to the Baer­ transferred the parasite from dogs to 2 foxes mann method. Hearts and lungs from some and a jackal (Canis aureus). Patent infections of the foxes were dissected . The right atrium were established in all 3 experimental ani­ and the pulmonary arteries were inspected mals (Guilhon 1965). According to our for adult parasites, but neither gross patho­ knowledge no experimental transfer from logical nor histopathological examinations wild foxes to dogs has ever been reported. were performed. In Denmark A. vasorum until recently had only been detected on necropsy of 2 dogs, Production ofinfective larvae both of which had visited France (Finnerup L1 were isolated by the Baermann method 1983, Monrad 1989). Over the last 2 years, from faeces of naturally infected foxes and however, clinical cases have been diagnosed dogs. The snails Biomphalaria glabrata and in a considerable number of Danish dogs, Helix pomatia (edible snail) were used as none of which have ever been outside Den­ intermediate hosts. Experimental infection mark (Koch 1992, Koch & Bolt 1990, Rosen of B. glabrata, was performed by adding L1 lund et al. 1991). Interestingly, all these cases to a beaker containing the snails according to have occurred north of Copenhagen, where the method described by Guilhon & de Gaa an endemic focus of yet unknown, but pos­ Ion (1969). Experimental infection of H. sibly growing extension seems to exist. This pomatia was performed in 2 steps. Firstly, suburban region is characterized by a dense each snail was fed a small piece of lettuce population of red foxes living in the immedi- contaminated with fluid containing L1 as Acta vel. scand, vol. 33 no. 4 • 1992 Angiostrongylosis in Denmark 359 described by Guilhon & Afghabi (1969), and Results secondly, each snail was placed on a water Wild foxe s film containing the L1 larvae in a beaker. In 12 of the 15 foxes typical A. vasorum L1 In order to demonstrate the development of were found in the faeces, though in moderate infective third-stage larvae (L3), the snails numbers « 150 Ll/g). Poor blood coagula­ were comminuted, and a proportion (10%) tion was observed in 4 of the infected foxes. of the snail tissue was digested in an Whenever infected foxes were necropsied, HClIpepsin solution at 30°C. Slightly modi­ adult A. vasorum of both sexes were found in fied versions of the techniques described by the right atrium of the heart and in the pul­ Wallace & Rosen (1969) were used. The L3 monary arteries. Few worms were found in recovered from the snails by digestion were each fox, and all foxes appeared to be in counted under a stereomicroscope. good bodily condition, indicating that the infection was of minor significance to the Infection offoxes and dogs foxes. Another 2 helminth species, Crenoso The final hosts were infected by feeding ma vulpis and Capillaria aerophila, were them infective snail material mixed with a found in 8 and 2 of the foxes, respectively. palatable feed. Two adult silver foxes (V. vulpes) originating from a fox farm were Experimental infection offoxes infected with L3 developed from Ll, which In the faeces from fox No.1 and fox No.2 had originally been isolated from the faeces excretion of A. vasorum L1 started 52 and 55 of a dog suffering from angiostrongylosis. days post infection , respectively. The foxes Fox No.1 received approximately 250 larvae were euthanized 74 days post infection . At passed in B. glabrata and fox No. 2 that time the faeces of fox No.1 and fox No. approximately 100 larvae passed in H. poma 2 contained 153 Ll/g and 1.5 Ll/g, respec­ tia. Another 2 uninfected foxes (No. 3 and tively. No clinical symptoms were noticed No.4), which were of the same origin as fox during the course of infection . At necropsy No.1 and No.2, served as non-infected con­ gross pathological lesions comparable to trols. The faeces of all 4 foxes were examined those described for naturally infected foxes by the Baermann method once a week. (Poli et al. 1985) and experimentally infected Two 4 month old SPF beagle puppies (dog dogs (Neff 1971, Prestwood et al. 1981) were No.1 and dog No.2) were infected, as well. found in the lungs of both foxes. A total of Dog No. 1 was infected with 100-200 L3 52 adult worms (28 females and 24 males) developed in B. glabrata from L1 isolated were found in fox No.1, whereas a total of 8 from the faeces of 2 wild red foxes. Dog No. adult worms (5 females and 3 males) were 2 was infected with 300-500 L3 developed in found in fox No.2. The faeces of fox No.3 B. glabrata from Ll isolated from the faeces and fox No.4 did at no time contain larvae, of 2 dogs suffering from angiostrongylosis. and no worms were found post mortem in Faeces from the dogs were examined by the these 2 foxes. Baermann method twice a week. Gross pathological lesions were noticed at Experimental infection ofdogs necropsy of foxes and dogs, while histopath­ In the faeces from dog No.1 and dog No.2 ological examination of lung tissue was car­ excretion of A.
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