Short CommunicationSeroprevalence of Neospora caninum in gray wolves in Scandinavia
Introduction
Neospora caninum is a protozoan parasite that was first described in dogs where it may cause paralysis of the hind limbs, ascending paresis, dermatitis, and other clinical symptoms (Buxton et al., 2002). Today it is also recognised as an important cause of bovine abortion (Dubey, 2003). N. caninum has a two-host lifecycle with dogs and coyotes (Canis latrans) as definitive hosts that can excrete oocysts in the faeces after ingestion of tissues from an infected intermediate host (McAllister et al., 1998, Gondim et al., 2004b). Many mammalian species can act as intermediate host for the parasite. Presence of N. caninum specific antibodies in blood indicates that the animal is, or has recently been, infected with the parasite (Björkman et al., 2007).
N. caninum infection in wildlife was first reported in 1994 when the parasite was identified in a black-tailed deer (Odocoileus hemionus columbianus) that had been found dead in California (Woods et al., 1994). Since then, serological evidence of N. caninum infection has been found in other wild herbivores, e.g. chamois (Rupicapra rupicapra), moose (Alces alces), red deer (Cervus elaphus), roe deer (Capreolus capreolus) and white-tailed deer (Odocoileus virginianus) (Dubey et al., 1999, Ferroglio and Rossi, 2001, Gondim et al., 2004a) but infection has not been proven by demonstration of the parasite. There is an ongoing discussion concerning the possibility that other wild canids than the coyote might serve as definitive hosts for N. caninum. Because of the very close relationship between the gray wolf (Canis lupus), the domestic dog, and the coyote, the gray wolf has been a top candidate as definitive host, and serological investigations indicate that they can be infected with the parasite (Gondim et al., 2004a, Dubey and Thulliez, 2005).
In Sweden, clinical disease associated with N. caninum has been reported in both dogs and cattle (Uggla et al., 1989b, Stenlund et al., 1997). Surveys have shown that 2% of the Swedish dairy cattle are infected with N. caninum and that 8% of the dairy herds house infected cows (Björkman et al., 2000, Frössling et al., 2008). The infected herds are not evenly distributed over Sweden but the prevalence is higher in the central parts of the country (Frössling et al., 2008). No demographic or other factors that might explain these regional differences have yet been identified, but it has been noticed that the high risk area for N. caninum infection in dairy cattle is located in a region which is inhabited by wolves.
The wolves in Sweden and Norway are members of a joint Scandinavian wolf population (Skandulv, 2009). After being nearly extinct in the beginning of 1970, the numbers have gradually increased and in the winter 2008–2009, the population was estimated at 213–252 individuals (Wabakken et al., 2009). The majority, 177–194 individuals in 2008–2009, live in family groups (packs) or pairs but there is also both migrating and stationary solitary wolves. The highest densities of wolves are found in south-central Sweden extending into Norway (58°2″–62°24″ N; 11°30″–16°43″ E).
The aim of this study was to estimate the seroprevalence of N. caninum in Scandinavian gray wolves and to investigate any geographical patterns of the infection.
Section snippets
Animals and samples
Blood samples used in this study were collected as part of the Scandinavian wolf monitoring project (Skandulv, 2009). Every winter since 1998–1999, wolves have been chemically immobilized for radio collaring, health assessment and collection of biological material. Some individuals have been captured several times to change the radio collar. Blood samples were collected from the cephalic vein, kept at room temperature for 1–2 h and then centrifuged at 1500 × g for 10 min. Serum was then separated
Results
Six of the 109 investigated wolves had serum samples with iscom ELISA COD ≥ 0.20 at the first sampling. Samples from four of the wolves were positive also in immunoblotting giving a N. caninum seroprevalence of 3.7% (95% CI: 0.1–7.2%). These seropositive animals were sampled in winter 2004–2005 in different packs. Twelve wolves were sampled for the first time this winter. Two of the seropositive wolves were males and two were females, and they were between 8 months and 5 years old (Table 1).
Discussion
The results of the present investigation indicate that N. caninum infection is present in Scandinavian wolves. It is unclear how the wolves in this study may have acquired the infection. Although we have not investigated presence of the parasite in prey species in this area, serological surveys indicate that N. caninum is very rare among Swedish wildlife. In a recent study comprising 417 moose sera collected from all over Sweden, all samples were negative (Malmsten et al., unpublished results).
Conflict of interest statement
The authors declare that they have no competing or conflicting interests.
Acknowledgement
We are grateful to Skandulv for giving us access to serum samples and information about the wolves included in this study.
References (25)
- et al.
Naturally occurring vertical transmission of Neospora caninum in dogs
Int. J. Parasitol.
(1998) - et al.
Neospora caninum and bovine virus diarrhoea virus infections in Swedish dairy cows in relation to abortion
Vet. J.
(2000) - et al.
The comparative pathogenesis of neosporosis
Trends Parasitol.
(2002) - et al.
High prevalence of antibodies to Neospora caninum in white-tailed deer (Odocoileus virginianus)
Int. J. Parasitol.
(1999) - et al.
Validation of a Neospora caninum iscom ELISA without a gold standard
Prev. Vet. Med.
(2003) Neospora caninum in wildlife
Trends Parasitol.
(2006)- et al.
Coyotes (Canis latrans) are definitive hosts of Neospora caninum
Int. J. Parasitol.
(2004) - et al.
Seroprevalences of Toxoplasma gondii and Neospora caninum in Swedish red foxes (Vulpes vulpes)
Vet. Parasitol.
(2001) - et al.
Encephalomyelitis and myositis in a boxer puppy due to a Neospora-like infection
Vet. Parasitol.
(1989) - Anonymous, 2009. Viltskadestatistik 2008. Viltskadecenter, pp. 1–30. On line:...
Neospora caninum in dogs: detection of antibodies by ELISA using an iscom antigen
Parasite Immunol.
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2016, Experimental ParasitologyCitation Excerpt :Also myocardial, pulmonary, dermatological and reproductive disorders could be present (Rasmussen and Jensen, 1996; Barber and Trees, 1998; Lyndsay et al., 1999; Dubey et al., 2007, 2011). N. caninum is an important cause of abortion in cattle (Dubey and Lindsay, 1996; Björkman et al., 2010) and it is widely distributed among bovine herds worldwide, where animals acquire the infection by ingesting food or water contaminated by the mature oocysts shed by dogs living in the same environment (Dubey and Schares, 2011). Despite canine hosts play a major role in the epidemiology of neosporosis, studies on the occurrence of the infection are still incipient in several areas.
A review of neosporosis and pathologic findings of Neospora caninum infection in wildlife
2015, International Journal for Parasitology: Parasites and WildlifeCitation Excerpt :Naturally occurring oocysts of N. caninum have been identified only in North American coyotes (Canis latrans) (Gondim et al., 2004b; Wapenaar et al., 2006), domestic dog–dingo hybrids living in remote Aboriginal communities in Australia (King et al., 2010, 2012), and gray wolves (C. lupus lupus) (Dubey et al., 2011). In addition to the above confirmed definitive hosts (Barber and Trees, 1996; Lindsay et al., 1996; Gondim et al., 2004a, 2004b; Dubey and Thulliez, 2005; Steinman et al., 2006; Wapenaar et al., 2007; Sobrino et al., 2008; Almberg et al., 2009; Bjorkman et al., 2010; Stieve et al., 2010; Bevins et al., 2013; Dubey et al., 2014a), N. caninum antibodies (Ab) and/or DNA have been detected in the following free-ranging carnivores: Iberian wolf (Canis lupus signatus) (Ab) (Sobrino et al., 2008), golden jackal (Canis aureus) (Ab) (Steinman et al., 2006), African wild dogs (Lycaon pictus) (Ab) (Woodroffe et al., 2012), red fox (Vulpes vulpes) (Ab, DNA) (Barber et al., 1997; Buxton et al., 1997; Simpson et al., 1997; Schares et al., 2001; Wolfe et al., 2001; Almeria et al., 2002; Hamilton et al., 2005; Hurkova and Modry, 2006; Steinman et al., 2006; Jakubek et al., 2007; Murphy et al., 2007; Wapenaar et al., 2007; Marco et al., 2008; Sobrino et al., 2008; De Craeye et al., 2011; Bartley et al., 2013b; Stuart et al., 2013; Dubey et al., 2014b), Culpeo fox (Dusicyon culpaeus) (Ab) (Martino et al., 2004), South American gray fox (Dusicyon griseus) (Ab) (Martino et al., 2004), North American gray fox (Urocyon cinereoenteus) (Ab) (Lindsay et al., 1996), Azara's fox (Lycalopex gymnocercus) (Ab) (Canon-Franco et al., 2004), crab-eating fox (Cerdocyon thous) (Ab) (Canon-Franco et al., 2004), European brown bear (Ursus arctos) (DNA) (Cobadiova et al., 2013), spotted hyena (Crocuta crocuta) (Ab) (Ferroglio et al., 2003), raccoon (Procyon lotor) (Ab, DNA) (Lindsay et al., 2001; Lemberger et al., 2005), raccoon dog (Nyctereute procyonoides) (Ab) (Kim et al., 2003), stone martin (Martes foina) (Ab) (Sobrino et al., 2008), pine martin (Martes martes) (Ab) (Sobrino et al., 2008), Eurasian badger (Meles meles) (Ab, DNA) (Sobrino et al., 2008; Bartley et al., 2013b), polecat (Mustella putorius) (Ab, DNA) (Sobrino et al., 2008; Bartley et al., 2013b), ferret (Mustela furo) (DNA) (Bartley et al., 2013b), American mink (Neovison vison) (Ab, DNA) (Bartley et al., 2013b; Stuart et al., 2013), European otter (Lutra lutra) (DNA) (Stuart et al., 2013), sea otter (Enhydra lutris neresis) (Dubey et al., 2003; Miller et al., 2010) common genet (Genetta genetta) (Ab) (Sobrino et al., 2008), Egyptian mongoose (Herpestes ichneumon) (Ab) (Sobrino et al., 2008; Millan et al., 2009), Eurasian wild cat (Felis silvestris silvestris) (Ab) (Sobrino et al., 2008), Iberian lynx (Lynx pardinus) (Ab) (Sobrino et al., 2008), cheetah (Acinonyx jubatus) (Ab) (Cheadle et al., 1999; Ferroglio et al., 2003), and lion (Panthera leo) (Ab) (Cheadle et al., 1999; Ferroglio et al., 2003). Viable N. caninum tachyzoites (isolates NcWolfMn1 and NcWolfMc2) have been recently isolated from the brains of two free-ranging gray wolves (Dubey et al., 2014a).
First molecular detection of Neospora caninum in European brown bear (Ursus arctos)
2013, Veterinary ParasitologyCitation Excerpt :From 29 brown bear (Ursus arctos) sera samples collected during the hunting season of 2001 in Scandinavia two sera tested positive, but the results were dubious since both sera were of bad quality and nonspecific cross-reactions could not be excluded (Åsbrink, 2002 ex. Björkman et al., 2010). European brown bear (Ursus arctos) is a large bear distributed across much of northern Eurasia and North America.
Detection of specific antibodies anti-Neospora caninum in the fallow deer (Dama dama)
2012, Research in Veterinary ScienceCitation Excerpt :None of examined sera produced positive bands characteristic for T. gondii antigen (data not shown). Extensive serological surveys demonstrated that N. caninum can infect a wide range of animal species worldwide (Dubey, 2003; Wolf et al., 2005; Björkman et al., 2010). The present study was conducted at field station where two species of wild ruminants were bred: European red deer and fallow deer.
Gray wolf (Canis lupus) is a natural definitive host for Neospora caninum
2011, Veterinary ParasitologyCitation Excerpt :Gondim et al. (2004a) proposed a sylvatic cycle of N. caninum in the US. N. caninum antibodies have been found in gray wolf in several countries including the US (Gondim et al., 2004b; Dubey and Thulliez, 2005; Steinman et al., 2006; Sobrino et al., 2008; Almberg et al., 2009; Björkman et al., 2010; Stieve et al., 2010; Dubey and Schares, in press). Almberg et al. (2009) found N. caninum antibodies in 50% of 220 wolves from the Yellowstone National Park, indicating efficient sylvatic cycle of N. caninum proposed by Gondim et al. (2004b).