Investigating the role of wild carnivores in the epidemiology of bovine neosporosis

Abstract

Neospora caninum is a protozoan parasite, primarily associated with bovine abortion. The only definitive hosts discovered to date are carnivores. This study aimed to identify the role of mammalian carnivores in the epidemiology of bovine neosporosis. A sample bank of serum, fecal and brain samples was established: American mink (Mustela vison), red foxes (Vulpes vulpes), pine martens (Martes martes), badgers (Meles meles), stoats (Mustela erminea), otters (Lutra lutra) and feral ferrets (Mustela putorius). Approximately 1% of mink and 1% of fox samples were positive by IFAT. According to PCR analysis of DNA extracted from brain tissue, 3% of the mink, 4% of the otters and 6% of the foxes examined were infected with N. caninum. All fecal samples tested negative for N. caninum DNA (n = 311), suggesting that the species that tested positive were intermediate not definitive hosts. This is the first time that tissues from mustelids have tested positive for N. caninum. The need to test 2 relatively large (~200 mg) targeted parts of the brain to avoid false negatives was also identified. The relatively low prevalence of N. caninum in Irish carnivores suggests that the local ecology of a species has an important influence on its epidemiological role.

A review of neosporosis and pathologic findings of Neospora caninum infection in wildlife

“…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 ...…”

“…Analysis of multiple tissues has been shown to increase the sensitivity of N. caninum detection and additional tissues in which N. caninum DNA has been commonly recognized include skeletal muscle, heart, liver, kidney, spinal cord, and lung ( Hughes et al., 2006; Ferroglio et al., 2007; Kang et al., 2009; Gondim et al., 2010; Sangster et al., 2010; Truppel et al., 2010; Bartley et al., 2013b; Medina-Esparza et al., 2013 ), with skeletal muscle and liver in rodents ( Ferroglio et al., 2007; Kang et al., 2009; Truppel et al., 2010; Medina-Esparza et al., 2013 ) and heart in sparrows ( Gondim et al., 2010 ) identified by some studies as the tissues most likely to be PCR positive for N. caninum . Studies have also shown that testing more than one section of brain significantly increases the likelihood of finding N. caninum DNA ( Hughes et al., 2008; Stuart et al., 2013 ). The tissue distribution of parasites in wildlife is not known, so to preclude underestimation of infection, we advise sampling multiple tissues (listed above) and at least two samples of brain to assess for N. caninum infection in molecular investigations.…”

Neospora caninumand Wildlife

“…As carnivores are at the top of the food chain, measuring their prevalence of N. caninum can give an indication of the presence of N. caninum infections lower down the food chain [ 62 – 64 ]. The level of N. caninum infection acquired by a carnivore will vary depending on the IH consumed [ 3 , 64 ].…”

Exposure of free-living jaguars to Toxoplasma gondii, Neospora caninum and Sarcocystis neurona in the Brazilian Pantanal

“…These domestic species are raised on cattle ranches and in rural communities in the Pantanal region on lands adjoining protected areas. As jaguars are at the top of the food chain, these findings may suggest that parasite infections occur further down the food chain (STUART et al, 2013), and that the role of predatorprey sentinels can be considered. However, further investigations involving this carnivore's ecology and prevalence within different species must be conducted in order to clarify this issue.…”