Wild and to estimate their reservoir competence based on

Wild animals are
obviously important for tick maintenance and long-term persistence of pathogens
often serving as a blood meal resource and reservoirs or amplification hosts,
respectively (Lorusso et al., 2011; Rizzoli et al., 2014). Among others, red
foxes are the most scrutinized wild carnivore species in Europe mostly because
of their high population densities and widespread distribution (Mitková et al.,
2017). As a result, they have been suggested as reservoirs for several TBPs
including those affecting companion animals and humans (Cardoso et al., 2015;
Hodži? et
al., 2015; Liesner et al., 2016; Ebani et al., 2017),
but their reservoir status has yet to be proven (Lorusso et al., 2011). The
main aim of the present project was to investigate the occurrence and genetic
diversity of tick-associated pathogens in foxes, and to estimate their
reservoir competence based on the data herein obtained and those available in
the published scientific literature.

To test our
hypothesis (H1), we analysed blood
and spleen samples from 506 foxes originating from two westernmost Austrian
provinces i.e., Tyrol and Vorarlberg for common pathogens derived by arthropod
vectors (Publication 1). As an
outcome of the comprehensive molecular study, it was found that foxes in
Austria harbour a substantial number of pathogenic agents of veterinary and
public health significance, and these include: Babesia canis, Babesia
cf. microti (syn. Theileria annae, Babesia microti-like, Babesia
vulpes), Hepatozoon canis, Anaplasma phagocytophilum, Candidatus Neoehrlichia sp. (FU98) and Bartonella rochalimae. Correspondingly
to the results of other studies from Europe (Duscher et al., 2014; Hodži? et
al., 2015; Tolnai et al., 2015; Ebani et al., 2017), Babesia cf. microti and H. canis were the most prevalent
pathogens in the foxes investigated. The high prevalence and wide geographic
range of these two haematozoan parasites infecting foxes nearly all over the
Europe are the main reasons why they have been proposed as a main reservoir
candidate. However, the high rate of infections itself does not necessarily
qualify the host as a reservoir (Rizzoli et al., 2014; Alvarado-Rybak et al.,
2016; Hodo and Hamer, 2017) and only indicates the exposure to the pathogen or
its carrier status (Estrada-Peña and de la Fuente, 2014; Hodo and Hamer, 2017).
Therefore, the reservoir role of a certain animal species can unequivocally be
demonstrated only through xenodiagnostic and transmission experiments (Rizzoli
et al., 2014). Unfortunately, such studies are rare and have not been performed
for most TBPs, so the reservoir status of wild animals, particularly
carnivores, involved in their natural transmission cycles still remains unknown
(Rizzoli et al., 2014). This mainly reflects the difficulties in long-term
keeping of wild animal colonies in captivity for experimental transmission
studies (Roque and Jansen, 2014). However, prevalence in combination with other
data provides a constructive framework for estimation the reservoir potential
in absence of such experimental studies (Gürtler and Cardinal, 2015; Hodo and
Hamer, 2017).

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The conceptual
approach has already been employed for assessing reservoir host competence and
the role of domestic and wildlife species in the transmission of Trypanosoma cruzi (Kinetoplastida:
Trypanosomatidae), and it can be applicable to any multihost pathogen
transmission system (Gürtler and Cardinal, 2015; Hodo and Hamer, 2017), including
Babesia cf. microti and H. canis.
Therefore, the results of the thesis are discussed in the light of the
following criteria: (1) host susceptibility, (2) host infectiousness to tick
vector, (3) tick-host contact, and (4) host-parasite haplotype associations.

(1) The relative
host susceptibility is defined as a proportion or probability of exposed animal
host to become infected, and it can be computed from the epidemiological
studies reporting the prevalence of infections (Hodo and Hamer, 2017). Babesia cf. microti and H. canis are
evidently the most common parasites hosted by red foxes in Europe, with an
overall rates of detection ranging from 1% (Zanet et al., 2014) to 69.2% (Cardoso
et al., 2013), and 7.8% (Farkas et al., 2014) to 100% (Criado-Fornelio et al.,
2003), respectively (Supplementary material). The large discrepancy in the
prevalence between the studies may be attributed to the geographic locality,
abundance and density of tick vectors, red fox population size and sensitivity
of PCR assays (Cardoso et al., 2013). However, the results of our study
revealed the infection rate highly depends on the tissue utilized for the
molecular detection. We observed that blood is statistically more frequently
infected with Babesia cf. microti compared to spleen, while spleen
exhibits the higher level of H. canis
infection than blood. Therefore, an aggregate overall prevalence of infection
i.e., total number of positive animals/total number of tested animals in all
published reports should be used for the comparative purposes (Hodo and Hamer,
2017) instead of the direct prevalence comparison since it is often deceptive (Gürtler
and Cardinal, 2015). Overall infection rate higher than 20% has been proposed
as one of the criteria used for reservoir host identification (Gürtler and
Cardinal, 2015). The aggregate overall prevalence of Babesia cf. microti and H. canis in foxes in Europe, calculated
from the available molecular genetic studies are estimated to be 23.9% and
28.4%, respectively (Supplementary material). Nonetheless, golden jackals (Canis aureus) and raccoon dogs (Nyctereutes procyonoides) are two other
wild carnivore species recently recognized as suitable hosts and potential
reservoirs for Babesia cf. microti (Mitková et al., 2017; Duscher
et al., 2017) and H. canis (Duscher
et al., 2013; Farkas et al., 2014; Mitková et al., 2017). However, their role
in the eco-epidemiology of the blood parasites is uncertain and requires more
in-depth studies involving larger number of samples from different geographical

(2) Furthermore,
capacity of a suspected reservoir host to infect a tick vector (host
infectiousness) is not equally distributed in the host population, and the
transmission pattern is mainly determined by host (e.g. genetic constitution,
body mass, sex, behaviour) and environmental factors (Hersh et al., 2012; Roque
and Jansen, 2014). Accordingly, the reservoir capacity of a given animal host
may be different at different localities and time points (Estrada-Peña and de
la Fuente, 2014). In absence of the xenodiagnostic surveys, the presence of a
parasite in the blood observed by cytology or PCR can be used as an indicator
to calculate the infectiousness index (Hodo and Hamer, 2017). The number of
studies in which blood has been used for the parasite detection in foxes is
considerably smaller compared to those using spleen, and showed an aggregate infectiousness
index for Babesia cf. microti and H. canis of 39.1% and 19.5%, respectively (Supplementary material).
Molecular detection of these two blood parasites by PCR is the gold standard
method for diagnosis of acute and chronic phase of the infections in dogs
(Otranto et al., 2011; Miró et al, 2015). The high level of parasitaemia in a
juvenile red fox naturally infected by H.
canis, with gamonts circulating in 60% of peripheral blood neutrophils has
recently been reported (Giannelli et al., 2017a). Moreover, the blood of the
particular fox was proven to be infective for Rhipicephalus turanicus, but not for Ixodes hexagonus and Haemaphysalis
erinacei ticks collected from the animal, which clearly denotes the host
infectiousness to the competent tick vector and further emphasized the fox
reservoir competence for H. canis.  


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