Babesia spp. in European wild ruminant species: parasite diversity and risk factors for infection

Abstract

Babesia are tick-borne parasites that are increasingly considered as a threat to animal and public health. We aimed to assess the role of European free-ranging wild ruminants as maintenance mammalian hosts for Babesia species and to determine risk factors for infection. EDTA blood was collected from 222 roe deer (Capreolus c. capreolus), 231 red deer (Cervus e. elaphus), 267 Alpine chamois (Rupicapra r. rupicapra) and 264 Alpine ibex (Capra i. ibex) from all over Switzerland and analysed by PCR with pan-Babesia primers targeting the 18S rRNA gene, primers specific for B. capreoli and Babesia sp. EU1, and by sequencing. Babesia species, including B. divergens, B. capreoli, Babesia sp. EU1, Babesia sp. CH1 and B. motasi, were detected in 10.7% of all samples. Five individuals were co-infected with two Babesia species. Infection with specific Babesia varied widely between host species. Cervidae were significantly more infected with Babesia spp. than Caprinae. Babesia capreoli and Babesia sp. EU1 were mostly found in roe deer (prevalences 17.1% and 7.7%, respectively) and B. divergens and Babesia sp. CH1 only in red deer. Factors significantly associated with infection were low altitude and young age. Identification of Babesia sp. CH1 in red deer, co-infection with multiple Babesia species and infection of wild Caprinae with B. motasi and Babesia sp. EU1 are novel findings. We propose wild Caprinae as spillover or accidental hosts for Babesia species but wild Cervidae as mammalian reservoir hosts for B. capreoli, possibly Babesia sp. EU1 and Babesia sp. CH1, whereas their role regarding B. divergens is more elusive.

Occurrence of Babesia species in captive reindeer (Rangifer tarandus) in Germany

“…B. venatorum is capable of causing zoonotic disease in immuncompromised humans (Herwaldt et al, 2003) and can infect roe deer, chamois and reindeer (Silaghi et al, 2011;Robert et al, 2008). Among European roe deer, asymptomatic infection appears to be common, as it has recently been recorded in Slovenia (Duh et al, 2005), France (Bastian et al, 2012), Italy (Tampieri et al, 2008;Zanet et al, 2014), Poland (Welc-Falęciak et al, 2013, Switzerland (Michel et al, 2014) and Germany (Overzier et al, 2013). In reindeer, however, clinical babesiosis caused by B. venatorum has been reported in Switzerland (Robert et al, 2008) and in the Netherlands (Kik et al, 2011).…”

“…Babesia divergens is known to cause acute disease in cattle (Bock et al, 2004) and humans (Skrabalo and Deanovic, 1957) and has been claimed to occur in asymptomatic roe deer, red deer, Chamois and Alpine ibex (Capra ibex) in Europe (e.g. Tampieri et al, 2008;Michel et al, 2014;Silaghi et al, 2011). Naturally acquired infection has also been described in reindeer before (Langton et al, 2003), but as mentioned above, the species identity of this sequence provided by Langton et al, (2003) is questionable as stated by Gray et al (2010).…”

“…In central Europe, high Babesia prevalences have been reported in free-ranging roe deer (Capreolus capreolus) in a forest in Bavaria, Germany (89.5%, Overzier et al, 2013), in various landscapes in Western France (58%, Bastian et al, 2012), in Northern and Central Italy (31%, Tampieri et al, 2008) and in the vicinity of Ljubljana, Slovenia (76.5%, Duh et al, 2005). Studies on a broader range of free-ranging wild ruminants have also shown Babesia infections in Switzerland (10.7%, Michel et al, 201413.6%, Hoby et al, 2009 and in Tyrol, Austria (17.9%, Silaghi et al, 2011).…”

The first detection of species of Babesia Starcovici, 1893 in moose, Alces alces (Linnaeus), in Norway

“…capreoli-like infection has been described in chamois (Hoby et al 2009). Several recently published reports have indicated that Babesia infection due to B. capreoli and B. venatorum may have contributed to the mortality of roe deer, reindeer and alpine chamois (Kik et al 2011, Michel et al 2014. Severe infections and Babesia-related mortalities were found in reindeer due to B. divergens and B. odocoilei (see Langton et al 2003, Barlett et al 2009).…”

“…Babesia venatorum has been identified in roe deer, Capreolus capreolus (Linnaeus) (Duh et al 2005, Bonnet et al 2007a. Babesia divergens and B. capreoli have been reported from roe deer, red deer, Cervus elaphus Linnaeus, reindeer, Rangifer tarandus (Linnaeus), alpine chamois, Rupicapra rupicapra (Linnaeus), and alpine ibex, Capra ibex (Linnaeus) (Langton et al 2003, Malandrin et al 2010, Zintl et al 2011, Michel et al 2014. However, the possible role of moose, Alces alces (Linnaeus), as a reservoir for Babesia spp.…”