Low circulation of TBEV in the studied site
TBEV was detected in nymph ticks from 2012 to 2014 with a very low
prevalence varying annually from 0.03% [95% CI: 0 – 0.15]) to
0.24% [95% CI : 0.07 – 0.62]. Although adult ticks are generally
more frequently infected than nymphs (Carpi, Bertolotti, Rosati, &
Rizzoli, 2009; Gaumann, Muhlemann, Strasser, & Beuret, 2010; Perez-Eid
et al., 1992; Rieille et al., 2014), our study did not detect the virus
in adult ticks. This could nonetheless be explained by our small sample
size. The method of collecting ticks by blanket dragging is more
suitable for collecting nymph ticks than for adult ticks of I.
ricinus . Considering the number of adults tested for TBEV, its
prevalence in adult ticks was estimated to be lower than 0.7%. These
estimations fit within the lower range values found in other studies in
Europe, ranging from <0.1 to 5% (Süss, 2011), and are similar
to those observed by Perez-Eid et al. (Perez-Eid et al., 1992) in the
Neuhof forest in Alsace between 1970 to 1974 with a maximum prevalence
of 0.12% [95% CI : 0.04 – 0.44] in nymphs and 0.77% [95% CI :
0.37 – 1.42] in adults.
In rodents, anti-TBEV antibodies were detected from 2012 to 2014 in 0%
- 5.2% of individuals per season. It is worth noting that TBEV
antibodies can only be detected during a short period between the
5th and the 13th day up to the
42nd day post-infection (Achazi et al., 2011; Milan
Labuda et al., 1997). This is consistent with the observed disappearance
of antibodies on seropositive animals captured a second time in our
study and the finding of seronegative animals carrying infected larvae.
These animals may have been recently infected and not yet seroconverted.
Therefore, TBEV seroprevalence in small mammals is a good proxy for the
occurrence of new infections in a month, although it is impossible to
distinguish antibodies due to maternal transfer from those developed
after a recent infection. In small mammals, maternal antibodies
generally last from 6 to 10 weeks (Gomez-Chamorro et al., 2019;
Grindstaff, Brodie, & Ketterson, 2003; Kallio et al., 2006) but this
duration is unknown for TBEV. We captured two juveniles aged 3-4 weeks
according to their weight that were seropositive. Considering the time
needed for seroconversion after an infection, these antibodies were
probably maternal antibodies. Although serological tests and sampling
design vary according to studies, the seroprevalence we observed in
2012-2015 is similar to that found by Perez-Eid et al. in Alsace
(Perez-Eid et al., 1992) (2.4%) and also fits within the lower values
found in western and central Europe (prevalence ranging from 1.6% to
23% (Achazi et al., 2011; Bakhvalova, Potapova, Panov, & Morozova,
2009; Caroline Burri et al., 2012; Cagnacci et al., 2012; Knap et al.,
2012; Kozuch, Gresíková, Nosek, Lichard, & Sekeyová, 1967; Tonteri et
al., 2011)). In 2012 and 2013, we also observed a small proportion of
rodents from which feeding ticks acquired the virus (2%) associated
with a low prevalence in feeding ticks (1.6%).
Our results in rodents and questing ticks therefore suggest a very low
circulation of TBEV in our site. This strengthens the hypothesis that
the virus circulates at a very low level in the natural foci of the
Alsace region, located at the western boundary of TBEV distribution.
Randolph et al. (S. E. Randolph et al., 1999) theorised that the
strength of TBEV enzootic cycles was influenced by the number of larvae
co-feeding with nymphs on small mammals. Like the results of Perez-Eid
et al. (Perez-Eid, 1990) in Alsace in the 1970s, we observed a very low
number of co-feeding ticks in June-July during the period of highest
tick activity, especially in 2012. We only captured 4.5% of rodents
infested by nymphs in 2012 when rodent abundance was high, whereas 17%
to 33% of rodents were reported to be infested by nymphs in
TBEV-infected sites in Switzerland and Slovakia (C. Burri et al., 2011;
S. E. Randolph et al., 1999). In addition, the mean infestation of
larvae per rodent-session infested by ticks (2.2) and per rodent-session
infested by nymphs (2) in 2012 was also lower than that observed in
other TBEV-infected sites (from 10 to 80 larvae per infested rodent and
from 5 to 65 larvae per host infested by nymphs) (C. Burri et al., 2011;
S. E. Randolph et al., 1999; Rosà et al., 2007). However, the apparent
difference in the number of feeding ticks in our study compared to other
field observations might be slightly lower considering that our method
for counting feeding ticks is not directly comparable with the methods
employed in other field studies and may have increased the
underestimation of the number of feeding ticks.