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In Europe, two tick species of the genus Dermacentor occur, Dermacentor marginatus and Dermacentor reticulatus. When the spatial distribution of both species in Germany was studied comprehensively for the first time in 1976, D. marginatus populations were recorded along the Rhine and Main river valleys in southwestern Germany, while D. reticulatus was very rare. In the last 50 years, however, a considerable range expansion of D. reticulatus has been noted in several European countries. To assess the current distribution of Dermacentor spp. in Germany, citizens were asked to send in ticks suspected to belong to the genus Dermacentor or that were of “unusual” appearance. From February 2019 until February 2020, 3,902 Dermacentor ticks were received in total. Of those, 15.48% (604/3,902) were identified as D. marginatus and 84.24% (3,287/3,902) as D. reticulatus, while 11 specimens could not be identified to species level. The majority of D. reticulatus specimens was collected from dogs (1,212/2,535; 47.12%), while D. marginatus was mostly collected from horses (184/526; 34.98%). Our results confirm that the adults of both Dermacentor species are active all year round. D. reticulatus specimens were sent in from all federal states except the Free and Hanseatic City of Hamburg, while D. marginatus specimens were only received from locations in southwestern Germany. Overall, data obtained from this citizen-science study show that D. reticulatus has significantly expanded its range, especially in northern Germany. Regarding D. marginatus, new locations northwest of the previous range were detected, although the distribution has remained rather stable as compared to D. reticulatus. The spread of D. reticulatus, the vector of Babesia canis, is of major importance for veterinarians and dog owners in terms of canine babesiosis outbreaks or endemization in hitherto B. canis-free areas. Thus, veterinarians and veterinary students need to be informed about the new situation to be able to give adequate advice to dog owners on the extended D. reticulatus range and appropriate control measures.
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ORIGINAL RESEARCH
published: 25 September 2020
doi: 10.3389/fvets.2020.578220
Frontiers in Veterinary Science | www.frontiersin.org 1September 2020 | Volume 7 | Article 578220
Edited by:
Anja Joachim,
University of Veterinary Medicine
Vienna, Austria
Reviewed by:
Riccardo Paolo Lia,
University of Bari Aldo Moro, Italy
Richard G. Robbins,
Walter Reed Biosystematics Unit
(WRBU), United States
*Correspondence:
Christina Strube
christina.strube@tiho-hannover.de
These authors have contributed
equally to this work
Specialty section:
This article was submitted to
Parasitology,
a section of the journal
Frontiers in Veterinary Science
Received: 30 June 2020
Accepted: 13 August 2020
Published: 25 September 2020
Citation:
Drehmann M, Springer A, Lindau A,
Fachet K, Mai S, Thoma D,
Schneider CR, Chitimia-Dobler L,
Bröker M, Dobler G, Mackenstedt U
and Strube C (2020) The Spatial
Distribution of Dermacentor Ticks
(Ixodidae) in Germany—Evidence of a
Continuing Spread of
Dermacentor reticulatus.
Front. Vet. Sci. 7:578220.
doi: 10.3389/fvets.2020.578220
The Spatial Distribution of
Dermacentor Ticks (Ixodidae) in
Germany—Evidence of a Continuing
Spread of Dermacentor reticulatus
Marco Drehmann 1†, Andrea Springer 2† , Alexander Lindau 1, Katrin Fachet 1, Sabrina Mai 1,
Dorothea Thoma 1, Carina R. Schneider 1, Lidia Chitimia-Dobler 1,3 , Michael Bröker 4,
Gerhard Dobler 1,3 , Ute Mackenstedt 1and Christina Strube 2
*
1Department of Parasitology, Institute of Biology, University of Hohenheim, Stuttgart, Germany, 2Institute for Parasitology,
Centre for Infection Medicine, University of Veterinary Medicine Hannover, Hanover, Germany, 3Bundeswehr Institute of
Microbiology, Munich, Germany, 4Global Health Press, Marburg, Germany
In Europe, two tick species of the genus Dermacentor occur, Dermacentor marginatus
and Dermacentor reticulatus. When the spatial distribution of both species in Germany
was studied comprehensively for the first time in 1976, D. marginatus populations were
recorded along the Rhine and Main river valleys in southwestern Germany, while D.
reticulatus was very rare. In the last 50 years, however, a considerable range expansion
of D. reticulatus has been noted in several European countries. To assess the current
distribution of Dermacentor spp. in Germany, citizens were asked to send in ticks
suspected to belong to the genus Dermacentor or that were of “unusual” appearance.
From February 2019 until February 2020, 3,902 Dermacentor ticks were received in
total. Of those, 15.48% (604/3,902) were identified as D. marginatus and 84.24%
(3,287/3,902) as D. reticulatus, while 11 specimens could not be identified to species
level. The majority of D. reticulatus specimens was collected from dogs (1,212/2,535;
47.12%), while D. marginatus was mostly collected from horses (184/526; 34.98%). Our
results confirm that the adults of both Dermacentor species are active all year round. D.
reticulatus specimens were sent in from all federal states except the Free and Hanseatic
City of Hamburg, while D. marginatus specimens were only received from locations
in southwestern Germany. Overall, data obtained from this citizen-science study show
that D. reticulatus has significantly expanded its range, especially in northern Germany.
Regarding D. marginatus, new locations northwest of the previous range were detected,
although the distribution has remained rather stable as compared to D. reticulatus.
The spread of D. reticulatus, the vector of Babesia canis, is of major importance for
veterinarians and dog owners in terms of canine babesiosis outbreaks or endemization
in hitherto B. canis-free areas. Thus, veterinarians and veterinary students need to be
informed about the new situation to be able to give adequate advice to dog owners on
the extended D. reticulatus range and appropriate control measures.
Keywords: Dermacentor reticulatus, Dermacentor marginatus, species distribution, Germany, range expansion,
citizen-science
Drehmann et al. Dermacentor Distribution in Germany
INTRODUCTION
In Europe, the hard tick genus Dermacentor is represented
by two species, Dermacentor marginatus (Sulzer, 1776) and
Dermacentor reticulatus (Fabricius, 1794). The range of the
ornate sheep tick, D. marginatus, extends from Portugal in the
west throughout southern Europe and northern Africa into
Central Asia. The species’ southern and northern distribution
limits are currently considered to be in Morocco and at the
northern extension of the Rhine basin in Germany (1). Within
this range, the species typically inhabits steppes, meadows, open
forests, and semi-desert areas (2). The ornate dog tick, D.
reticulatus, has a more northern distribution, occurring from
northern Portugal to southern Latvia (1). It is found in a wide
range of habitats, including meadows, open forests, heath-, and
marshland, clearings, and suburban wasteland (3).
Immature stages of both D. marginatus and D. reticulatus
are almost exclusively endophilic parasites of rodents. As
adults, both sexes commonly infest larger mammals such as
sheep, dogs, horses, goats, cattle (2), and occasionally humans
(4). They play a role as vectors of various pathogens of
considerable veterinary and medical importance. For example,
both D. marginatus and D. reticulatus are competent vectors
of protozoa of the order Piroplasmida, which may cause
potentially fatal disease in animals. The most important
causative agent of canine babesiosis in Europe, Babesia canis,
is transmitted by D. reticulatus (5), while both Dermacentor
species may transmit causative agents of equine piroplasmosis
(6). Additionally, the vector function of D. reticulatus for tick-
borne encephalitis virus (TBEV) has recently been proven (7).
Although Ixodes ricinus (Linnaeus, 1758) is the main vector
for TBEV in Europe, the virus has repeatedly been isolated
from D. reticulatus in a TBEV-endemic area in Germany (8).
Furthermore, Dermacentor spp. are the most relevant vectors for
two causative agents of tick-borne lymphadenopathy in central
Europe, Rickettsia slovaca transmitted by D. marginatus and
R. raoultii transmitted by D. reticulatus (2,3). In addition,
both species are relevant in central Europe as vectors of
Francisella tularensis (9), and D. marginatus may contribute
to the transmission of Coxiella burnetii, the causative agent of
zoonotic Q fever (10).
The first comprehensive study on the spatial distribution of
the genus Dermacentor in Germany was published by Liebisch
and Rahman (11). The authors reported a mosaic-like pattern
of D. marginatus occurrence along the Rhine and Main river
valleys in southwestern Germany. In contrast, an established
D. reticulatus population was found at only one location in
Germany at that time, in a forest near Tübingen. In the 1960s,
D. reticulatus was also reported from the area of Potsdam in
the former German Democratic Republic (12). In the recent
past, comprehensive data on the distribution of both species
in Germany have been gathered from either citizen-science
approaches (13) or literature reviews (1,14). These data,
including reports on Dermacentor occurrence up to the year
2014, showed a considerable range expansion of D. reticulatus,
which is in accordance with reports from other European
countries, e.g., Slovakia and Poland (15,16).
In 2019, we received indications of a further significant spread
of D. reticulatus in Germany and thus aimed to assess the current
distribution of D. reticulatus and D. marginatus in Germany by
involving the general public. Citizens were asked to send in ticks
belonging to the genus Dermacentor or of unusual appearance to
allow mapping the distribution of both Dermacentor species in
detail and identifying new areas of occurrence.
MATERIALS AND METHODS
Citizen-Science Call
In February 2019, a single male specimen of D. reticulatus
collected from a dog in the city of Hanover, northern Germany,
was received by the Institute for Parasitology, University of
Veterinary Medicine Hannover. This was an unusual finding,
as hitherto the region of Hanover has not been considered
within the range of this tick species. Upon request, the owner
stated that the tick was found crawling on the dog after a
walk and that the dog had not traveled recently. Additionally,
in March 2019, a member of the institute noticed one female
and three male Dermacentor ticks on her dog after a walk in
Clausthal-Zellerfeld, located about 75 km southeast of Hanover,
also hitherto not recognized as within the German Dermacentor
range. To investigate whether these were accidental findings or
if a further range expansion of D. reticulatus has occurred in
Germany, a call to send in Dermacentor ticks was published in the
May issue of the gazette of the Federal Chamber of Veterinarians,
which is sent to every veterinarian in Germany. Furthermore, a
press release was issued at the beginning of May 2019, asking
citizens to send in Dermacentor ticks, which was shared through
several print and social media.
Additionally, as of the end of February 2019, the Department
of Parasitology at the University of Hohenheim near Stuttgart,
southern Germany, released a call to send in Hyalomma ticks
as well as ticks of unusual appearance. Again, respective press
releases were circulated in various regional and national media,
and, additionally, a website was designed for further information,
where citizens were also specifically asked to send in ticks of the
genus Dermacentor.
All media releases included pictures to help citizens
distinguish between different tick genera. Along with the ticks,
citizens were asked to provide information on the date and
location of collection [Global Positioning System (GPS) data
or postal code], the involvement of potential hosts, and details
about the circumstances under which the tick was discovered. To
increase motivation to participate, citizens were informed about
the tick species of their specimen(s).
Tick Identification and Geographical
Classification
Ticks were identified to species level using detailed morpho-
metrical keys provided by Arthur (17), Siuda (18), and Estrada-
Peña et al. (19).
The accuracy of the reported locations where ticks were found
was categorized based on the details provided by the senders
as follows: (i) the accuracy was estimated to be high if there
was a high probability that a natural habitat of the collected
Frontiers in Veterinary Science | www.frontiersin.org 2September 2020 | Volume 7 | Article 578220
Drehmann et al. Dermacentor Distribution in Germany
FIGURE 1 | Distribution of Dermacentor reticulatus (A) and Dermacentor marginatus (B) in Germany based on ticks submitted by German citizens from February
2019 to February 2020. Only locations with medium to high accuracy are shown (D. reticulatus:N=1,744/3,287, D. marginatus:N=450/604). More intense colors
indicate multiple findings in close proximity. Red shaded areas in (A) represent areas of D. reticulatus distribution as reported by the European Centre for Disease
Prevention and Control (ECDC) in July 2019 (https://www.ecdc.europa.eu/en/publications-data/dermacentor-reticulatus-current- known-distribution- july-2019) for
comparison. In the map insert, federal states are abbreviated with italic letters (B, Berlin; BR, Bremen; BW, Baden-Wuerttemberg; BV, Bavaria; BB, Brandenburg; HH,
Free and Hanseatic City of Hamburg; H, Hesse; LS, Lower Saxony; MWP, Mecklenburg-Western Pomerania; NRW, North Rhine-Westphalia; RP,
Rhineland-Palatinate; S, Saxony; SA, Saxony-Anhalt; SH, Schleswig-Holstein; SL, Saarland; T, Thuringia). Cities are abbreviated with bold letters (BS, Brunswick; C,
Cologne; F, Freiburg; G, Gießen; H, Hanover; K, Karlsruhe; L, Leipzig; M, Mannheim; S, Stuttgart).
tick was in close proximity to the location where it was found.
For example, a high accuracy was assumed for ticks collected
from cattle and horses, which did not leave their pasture in
the days before an infestation was detected, as well as for ticks
found on vegetation, but only when the sender provided a
GPS reference or precise address. (ii) A medium accuracy was
assumed for unengorged ticks found on dogs or humans during
or immediately after a walk, as well as for ticks from cats or wild
terrestrial animals, or if the location met the criteria for a high
accuracy ranking but was reported only in the form of a postal
code. (iii) The reported location was considered to be of low
accuracy in cases of engorged ticks found on dogs or ticks found
in an unsuitable habitat (e.g. inside a house), as the origin of these
ticks was often unclear. (iv) If no information on the location
or the circumstances of tick detection was provided or the ticks
were detected on dogs or humans travelling large distances, the
accuracy was categorized as unknown.
Only locations with a high or medium accuracy were used for
distribution maps. These distribution maps were compared with
the results reported by Rubel et al. (1) and Naucke (13). Maps
were generated in R v. 3.5.1 (20) with spatial data retrieved via
the rworldmap package (21), via the eurostat package (22), and
from the Global Administrative Areas Database (23).
RESULTS
Tick Collection and Identification
From mid-February 2019 until the end of February 2020,
3,902 ticks of the genus Dermacentor were received. With a
total of 3,287 (84.24%) specimens, D. reticulatus was sent in
much more frequently than D. marginatus (604 specimens;
15.48%). The remaining 11 specimens (0.28%) could not be
identified to species level, as essential morphological features had
been destroyed. The sex ratio of D. reticulatus was almost 1:1
[48.65% females (1,599/3,287) vs. 51.32% males (1,687/3,287)].
In addition, one D. reticulatus nymph was received (0.03%). In
contrast, slightly more female than male D. marginatus were sent
in [56.79% females (343/604) vs. 43.21% males (261/604)].
Geographic Distribution
For 3,877/3,902 ticks, the federal state of origin was
unambiguous, whereas for 24 D. reticulatus and one D.
marginatus, the federal state of origin was unclear due to travel
activity of the senders. With the exception of the Free and
Hanseatic City of Hamburg, D. reticulatus was collected in
all federal states of Germany (Figure 1A). The number of D.
reticulatus exceeded the number of D. marginatus received from
Frontiers in Veterinary Science | www.frontiersin.org 3September 2020 | Volume 7 | Article 578220
Drehmann et al. Dermacentor Distribution in Germany
TABLE 1 | Distribution of the 3,263 Dermacentor reticulatus, 603 Dermacentor
marginatus, and 11 unidentified Dermacentor specimens of unambiguous origin
among the federal states of Germany.
Federal state D. reticulatus D. marginatus Dermacentor spp.
Baden-
Wuerttemberg
25.84% (843/3,263) 36.32% (219/603) 9.09% (1/11)
Bavaria 1.72% (56/3,263) 3.32% (20/603) 0.00% (0/11)
Berlin 1.47% (48/3,263) 0.00% (0/603) 0.00% (0/11)
Brandenburg 14.40% (470/3,263) 0.00% (0/603) 18.18% (2/11)
Free Hanseatic
City of Bremen
0.03% (1/3,263) 0.00% (0/603) 0.00% (0/11)
Free and
Hanseatic City of
Hamburg
0.00% (0/3,263) 0.00% (0/603) 0.00% (0/11)
Hesse 7.26% (237/3,263) 7.13% (43/603) 0.00% (0/11)
Lower Saxony 18.57% (606/3,263) 0.00% (0/603) 45.45% (5/11)
Mecklenburg-
Western
Pomerania
0.83% (27/3,263) 0.00% (0/603) 0.00% (0/11)
North
Rhine-Westphalia
1.47% (48/3,263) 2.65% (16/603) 0.00% (0/11)
Rhineland-
Palatinate
2.60% (85/3,263) 50.25% (303/603) 9.09% (1/11)
Saarland 1.29% (42/3,263) 0.33% (2/603) 0.00% (0/11)
Saxony 16.24% (530/3,263) 0.00% (0/603) 0.00% (0/11)
Saxony-Anhalt 4.57% (149/3,263) 0.00% (0/603) 9.09% (1/11)
Schleswig-
Holstein
0.21% (7/3,263) 0.00% (0/603) 0.00% (0/11)
Thuringia 3.49% (114/3,263) 0.00% (0/603) 9.09% (1/11)
each federal state, except for Rhineland-Palatinate, where D.
marginatus was collected more frequently (Table 1,Figure 1B).
In contrast to D. reticulatus,D. marginatus specimens were
received from only six federal states located in southern and
western Germany (Baden-Wuerttemberg, Bavaria, Hesse, North
Rhine-Westphalia, Rhineland-Palatinate, and Saarland) (Table 1,
Figure 1). Compared with the distribution maps provided by
Rubel et al. (1) and Naucke (13), several additional sites of D.
reticulatus occurrence are evident, especially in the north of
Germany (Figure 2A). The spatial distribution of D. marginatus
is largely comparable to the data provided by Rubel et al. (1)
and Liebisch and Rahman (11). However, additional areas
of occurrence were identified, for example, in the vicinity of
Cologne (Figure 2B).
Temporal Course of Citizens’ Dermacentor
Collections
For 2,785/3,287 D. reticulatus and 596/604 D. marginatus
specimens, information on the month of collection was provided.
Both Dermacentor species occurred throughout the whole
year. Most D. reticulatus specimens were found in September
(940/2,785; 33.75%) and October 2019 (666/2,785; 23.91%),
while smaller peaks occurred in March 2019 (187/2,785, 6.71%;
following the press release by the University of Hohenheim),
May 2019 (156/2,785, 5.60%; following the press release by
the University of Veterinary Medicine, Hanover), and February
2020 (234/2,785, 8.40%). In comparison, D. marginatus numbers
showed a peak in March 2019 (157/596; 26.34%) and February
2020 (199/596; 33.39%) (Figure 3).
Host Association
Information on host association was available for 3,061/3,902
ticks (2,535/3,287 D. reticulatus and 526/604 D. marginatus). The
majority of ticks were attached to or crawling on (potential) hosts,
especially dogs (1,233/3,061; 40.28%) and horses (608/3,061;
19.86%). While D. reticulatus was collected more often from dogs
(1,212/2,535; 47.81%) than from horses (423/2,535; 16.69%), D.
marginatus was more common on horses (184/526; 34.98%) than
on dogs (16/526; 3.04%). Both species were also detected on
humans [D. reticulatus: 110/2,535 (4.34%); D. marginatus: 66/526
(12.55%)]. In 18 cases, citizens reported having been bitten by
the ticks [nine times by D. marginatus (1.71%), nine times by
D. reticulatus (0.36%)]. These ticks were often attached to the
scalp. Detailed results on host association or collection location,
respectively, are shown in Table 2.
DISCUSSION
The present study aimed to assess the current distribution of
Dermacentor spp. in Germany. A continuing range expansion of
D. reticulatus has been observed in several European countries
(2426). This range expansion has been attributed to climatic
changes as well as changes in land use, travel activities of
humans and pets, and an increase in available wildlife hosts,
e.g., red foxes and wild boar (3). The spread of D. reticulatus
is of considerable veterinary importance, since it is the vector
of Babesia canis, a life-threatening protozoan blood parasite of
dogs. Currently, B. canis transmission only occurs in restricted
areas in Germany (27,28), while autochthonous infections with
other piroplasms transmitted by Dermacentor spp., such as B.
caballi and T. equi causing equine piroplasmosis, are rare in
Germany (29). Nevertheless, introduction of these pathogens
with infected animals or ticks from endemic areas may lead
to the emergence of new transmission foci in areas where
Dermacentor populations are present, especially since Babesia
spp. are transmitted transovarially in ticks (30). Furthermore,
D. reticulatus may pose a risk for humans due to its vector role
for R. raoultii,F. tularensis, and TBEV, among other tick-borne
pathogens (2,3).
Although D. reticulatus is considered to have been part
of the German tick fauna for at least 100 years (31), it was
limited to only few reported locations during most of the 20th
century (12,32,33). After 1976, D. reticulatus apparently started
spreading probably from at least two different populations,
one in southwestern (11) and one in northeastern Germany
(12). In the 1990s, several previously unknown D. reticulatus
populations were described following autochthonous cases of
canine babesiosis (28,34), although comprehensive studies on the
species’ distribution during the last quarter of the 20th century
are lacking. Since the turn of the millennium, the distribution of
Frontiers in Veterinary Science | www.frontiersin.org 4September 2020 | Volume 7 | Article 578220
Drehmann et al. Dermacentor Distribution in Germany
FIGURE 2 | Distribution of (A) Dermacentor reticulatus (blue dots) and (B) Dermacentor marginatus (red dots) in Germany based on ticks submitted by German
citizens from February 2019 to February 2020 in comparison to data from previous studies. In (A),D. reticulatus locations as reported by Rubel et al. (1) are shown in
orange and those reported by Naucke (13) in green. In (B) D. marginatus locations as reported by Rubel et al. (1) are shown in yellow. More intense colors indicate
multiple findings in close proximity. In the map insert, federal states are abbreviated with italic letters (B, Berlin; BR, Bremen; BW, Baden-Wuerttemberg; BV, Bavaria;
BB, Brandenburg; HH, Free and Hanseatic City of Hamburg; H, Hesse; LS, Lower Saxony; MWP, Mecklenburg-Western Pomerania; NRW, North Rhine-Westphalia;
RP, Rhineland-Palatinate; S, Saxony; SA, Saxony-Anhalt; SH, Schleswig-Holstein; SL, Saarland; T, Thuringia). Cities are abbreviated with bold letters (BS, Brunswick;
C, Cologne; F, Freiburg; G, Gießen; H, Hanover; K, Karlsruhe; L, Leipzig; M, Mannheim; S, Stuttgart).
FIGURE 3 | Dermacentor reticulatus (N=2,785) and Dermacentor marginatus (N=596) specimens by month of collection, sent in by German citizens from February
2019 to February 2020.
D. reticulatus in Germany has been the subject of several studies,
especially with regard to its increased spread (1,13,32,35,36). As
compared to field studies or literature surveys, studies involving
citizens can cover a wider spatial extent and result in a larger
number of records (37,38), although the quality of the obtained
data can be variable.
Frontiers in Veterinary Science | www.frontiersin.org 5September 2020 | Volume 7 | Article 578220
Drehmann et al. Dermacentor Distribution in Germany
TABLE 2 | Host association or location of collection for the subset of
Dermacentor ticks for which this information was available.
Host/location D. reticulatus D. marginatus Dermacentor spp.
Alpaca 0.00% (0/2,535) 0.95% (5/526) 0.00% (0/8)
Cat 0.63% (16/2,535) 0.19% (1/526) 0.00% (0/8)
Cattle 0.16% (4/2,535) 1.14% (6/526) 0.00% (0/8)
Dog 47.81% (1,212/2,535) 3.04% (16/526) 62.50% (5/8)
Donkey 0.00% (0/2,535) 29.28% (154/526) 0.00% (0/8)
Horse 16.69% (423/2,535) 34.98% (184/526) 12.50% (1/8)
Human 4.34% (110/2,535) 12.55% (66/526) 12.50% (1/8)
Moufflon 0.08% (2/2,535) 0.00% (0/526) 0.00% (0/8)
Raccoon dog 0.04% (1/2,535) 0.00% (0/526) 0.00% (0/8)
Wild boar 2.09% (53/2,535) 1.14% (6/526) 0.00% (0/8)
Car 0.24% (6/2,535) 0.57% (3/526) 0.00% (0/8)
Textiles 3.12% (79/2,535) 3.42% (18/526) 0.00% (0/8)
Garden 0.47% (12/2,535) 1.14% (6/526) 0.00% (0/8)
Indoors 5.60% (142/2,535) 7.98% (42/526) 12.50% (1/8)
Outdoors 18.74% (475/2,535) 3.61% (19/526) 0.00% (0/8)
In the current study, only records presumably reflecting the
true occurrence of the tick species, i.e., those assigned to a
high or medium geographic accuracy, were taken into account
for distribution maps. Our results confirm earlier studies (1,
13,32), indicating that D. reticulatus is continuing its spread
throughout Germany.
When compared with the most recent data provided by
the European Centre for Disease Prevention and Control (39)
(ECDC, cf. Figure 1A), our results show that multiple new
foci of D. reticulatus occurrence have appeared in northern,
western, and southern Germany. However, the comparability of
the ECDC’s map with the data generated in the present study
is limited, as the resolution of the map provided by the ECDC
is based on government districts and is therefore comparatively
low (39).
The obtained data show notable clusters of D. reticulatus
occurrence around the cities of Hanover and Brunswick (eastern
part of the northern German federal state of Lower Saxony),
Stuttgart, Mannheim, Freiburg, and Karlsruhe (western part of
the southern German federal state of Baden-Wuerttemberg). In
this context, however, it has to be kept in mind that citizens were
asked to participate in the study via press releases, which were
covered by various regional and national media. Regional media
coverage was probably enhanced in the vicinity of the involved
research institutions (located in Hanover and Stuttgart); thus,
the clusters near Hanover and Stuttgart may reflect this bias in
media attention. Nevertheless, D. reticulatus was detected for the
first time in the greater Hanover area, where occurrence was also
verified by flagging of questing ticks in 2019 (data not shown). In
addition, the data indicate several other potentially new locations
outside the hitherto known range, especially in northwestern
Germany. D. reticulatus was even found in the northernmost
part of Germany, on the island of Sylt in the North Sea (8.34
E/54.91N). Two independent submissions of unfed male ticks
from Sylt indicate that a D. reticulatus population may be present
on the island. However, Sylt is also a popular tourist destination,
and it cannot be entirely excluded that the unfed male ticks did
not originate on the island, but reached it together with traveling
dog hosts.
A further cluster of D. reticulatus occurrence was noted
in the eastern part of Germany, around the federal state of
Berlin. Interestingly, the citizen-science data do not confirm
the presence of D. reticulatus in the area between the cities of
Leipzig and Berlin, where the species was previously reported
(1,32). However, this may be due to the low population density
in this area, limiting the number of participants in the study.
Alternatively, D. reticulatus may be so widespread in this region
that the local population did not consider respective findings
worth reporting.
The distribution of D. marginatus as indicated by this study is
still very similar to the data presented by Liebisch and Rahman
(11), also included in the distribution map by Rubel et al. (1).
Nevertheless, additional locations were found in the federal state
Rhineland-Palatine and in North Rhine-Westphalia, near the city
of Cologne (6.96E/50.94N). To date, the current northern
distribution limit of D. marginatus was believed to be near
Giessen, federal state of Hesse, Germany, at coordinates 8.32
E/50.65N (40). Thus, a slight northward spread, probably along
the Rhine, did occur. Interestingly, the ecological niche model
by Walter et al. (40) identified most of Rhineland-Palatinate as
suitable habitat for D. marginatus, as well as a large area to the
northeast of the distribution limit, including the entire federal
state of Hesse and even the southern part of Lower Saxony.
In contrast, North Rhine-Westphalia, which is located to the
northwest of Giessen, was not identified as a suitable habitat by
Walter et al. (40). Further studies should continue to examine
whether stable populations of D. marginatus are permanently
established in North Rhine-Westphalia.
The seasonal activity of both Dermacentor species in Central
Europe was studied multiple times in the past (2,3). The data
presented here accord with former reports (41), as D. reticulatus
numbers in Germany peaked in September and October and,
to a lesser extent, from March to May, whereas D. marginatus
numbers peaked in February and March. Similar patterns were
observed in field studies on questing Dermacentor ticks in other
parts of Europe [e.g. (42,43)]. Likewise, the current study
confirms winter activity of both tick species (3,43). However, it
must be kept in mind that media coverage and human behavior,
among other factors, can bias data gathered by a citizen-science
approach, which limits the comparability to data from field
collections. Sendings in March and May 2019 were probably
influenced by the preceding press releases issued by the involved
research institutions.
D. reticulatus was found predominantly on dogs, whereas
D. marginatus was found mostly on equids. Among domestic
animals, adult D. reticulatus seems to prefer dogs and may even
outnumber I. ricinus on these hosts in areas where both species
occur (44). In contrast, the main hosts of adult D. marginatus are
ungulates, especially sheep (11). The fact that no D. marginatus
was collected from sheep in the present study may be attributed
to the study design, as horse or dog owners are far more likely
to notice Dermacentor ticks on their animals as something
Frontiers in Veterinary Science | www.frontiersin.org 6September 2020 | Volume 7 | Article 578220
Drehmann et al. Dermacentor Distribution in Germany
unusual and worth reporting than shepherds, who probably do
not consider D. marginatus ticks as unusual. In addition, sheep
are probably less often checked for tick infestation than dogs
or horses, and their thick wool makes ticks hard to spot if the
infestation is not severe.
In light of the zoonotic pathogens that may be transmitted
by Dermacentor spp., it is worth noting that human tick bites
were only rarely reported. Although 4.34% of D. reticulatus
and 12.55% of D. marginatus for which information on host
association was provided were found crawling on humans, the
proportions of ticks that had actually bitten humans were only
0.36 and 1.71%, respectively. In Spain, where both D. reticulatus
and D. marginatus occur, these species accounted for 2.22 and
12.52% of 4,049 ticks found on humans, respectively (4). These
numbers are comparable to our data; however, no information on
the proportion of ticks that had actually bitten humans appears
in the Spanish study. In the areas of Liguria and Tuscany, Italy,
D. marginatus was identified as the second most important
anthropophagic tick, after I. ricinus, accounting for 9.1% of 565
human tick bites (45). In contrast, among 2,547 ticks removed
from humans in Germany between 2013 and 2017, only 0.16%
were identified as Dermacentor spp. (46). Overall, the available
data indicate that D. marginatus is more likely to attach to or even
bite humans than D. reticulatus.
CONCLUSIONS
The present study shows that D. reticulatus is continuing to
spread in Germany, especially in the northwestern part of the
country. Overall, this tick was found in all federal states except the
Free and Hanseatic City of Hamburg. In contrast, the distribution
of D. marginatus is still restricted to southwestern Germany;
however, newly identified locations in North Rhine-Westphalia
show that this species has also undergone a geographical spread.
A range expansion of both species is particularly worrying
in light of their role as vectors. Both species may transmit
human pathogens; however, they rarely seem to bite humans
in Germany. Thus, the implications for public health may be
considered of minor importance. By contrast, the spread of
D. reticulatus is of major importance for veterinarians and dog
owners in terms of canine babesiosis outbreaks or endemization
in hitherto B. canis-free areas. Thus, veterinarians and veterinary
students need to be informed about this situation, with updates
during continuing education. Similarly, dog owners need to be
advised on the expanding D. reticulatus range and the need
for careful tick control measures by veterinarians and, where
appropriate, by veterinary associations such as the German
chapter of the European Scientific Counsel Companion Animal
Parasites (ESCCAP).
DATA AVAILABILITY STATEMENT
The original contributions presented in the study are included
in the article/supplementary material, further inquiries can be
directed to the corresponding author/s.
AUTHOR CONTRIBUTIONS
CS, GD, UM, MD, AS, and AL designed the study. UM and
CS coordinated the study and communicated with media
representatives. MD designed the website. LC-D, MB, and
GD contributed collected ticks. AS, MD, AL, KF, and LC-D
identified tick species. AS, MD, AL, KF, SM, DT, and CRS
participated in communication with the public and individual
citizens as well as data handling. MD and AS drafted the
manuscript. All authors participated in data interpretation,
reviewed the manuscript draft, read, and approved the
final manuscript.
FUNDING
AS and CS were supported by a grant of the European Union
through the European Regional Development Fund and the
Interreg North Sea Region Programme 2014–2020 as part of the
NorthTick project (reference number J-No. 38-2-7-19).
ACKNOWLEDGMENTS
The authors would like to thank all citizens participating in this
study for their valuable support.
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Conflict of Interest: The authors declare that the research was conducted in the
absence of any commercial or financial relationships that could be construed as a
potential conflict of interest.
Copyright © 2020 Drehmann, Springer, Lindau, Fachet, Mai, Thoma, Schneider,
Chitimia-Dobler, Bröker, Dobler, Mackenstedt and Strube. This is an open-access
article distributed under the terms of the Creative Commons Attribution License (CC
BY). The use, distribution or reproduction in other forums is permitted, provided
the original author(s) and the copyright owner(s) are credited and that the original
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No use, distribution or reproduction is permitted which does not comply with these
terms.
Frontiers in Veterinary Science | www.frontiersin.org 8September 2020 | Volume 7 | Article 578220
... During the last two decades, an increasing number of studies has reported marked habitat expansion of the ornate dog tick, Dermacentor reticulatus, in several European countries, including Poland (3,4), Slovakia (5), the Czech Republic (6), the United Kingdom (7), the Netherlands (8), and Germany (9,10). This tick species plays an important role in veterinary medicine due to its vector function for Babesia canis, the piroplasmid parasite responsible for potentially fatal babesiosis in dogs (11). ...
... reticulatus are probably multi-factorial, involving changes in agricultural practices and land use, such as renaturation of landscapes, increased density and movement of wildlife and domestic animals as well as increased temperatures, which facilitate the completion of the tick's life cycle within 1-2 years (17)(18)(19)(20). In contrast to D. reticulatus, the range of the only congeneric species in Europe, Dermacentor marginatus, seems to be rather stable, although a possible northward expansion along the Rhine has recently been reported (10). In 2019, a citizen science study was initiated in Germany to collect data on the geographic distribution of Dermacentor ticks (10). ...
... In contrast to D. reticulatus, the range of the only congeneric species in Europe, Dermacentor marginatus, seems to be rather stable, although a possible northward expansion along the Rhine has recently been reported (10). In 2019, a citizen science study was initiated in Germany to collect data on the geographic distribution of Dermacentor ticks (10). The study has been continued since and allows an update of the reported distribution, with several new locations with Dermacentor infestation risk. ...
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A considerable range expansion of Dermacentor reticulatus has been observed in several European countries, which is concerning in the light of its vector function for several pathogens, including Babesia canis and tick-borne encephalitis virus (TBEV). The present study provides an update on the distribution of Dermacentor ticks in Germany, using a citizen science approach. Ticks were collected by citizens from March 2020 to May 2021, and submitted along with information on the date and location of collection, potential hosts and details about the circumstances of discovery. In total, 3,292 Dermacentor specimens were received, of which 76.4% (2,515/3,292) were identified as D. reticulatus and 23.0% (758/3,292) as D. marginatus, while 0.6% (19/3,292) were too damaged for species-level identification. Dermacentor reticulatus was received from all federal states of Germany. Maxent species distribution models predicted suitable environmental conditions for D. reticulatus throughout Germany. Findings on the vegetation or on pastured animals without travel history confirmed the occurrence of this tick species as far north as the most northern German federal state Schleswig-Holstein. In contrast, the distribution of D. marginatus still appears to be limited to southwestern Germany, although the northward shift of the distribution limit observed in the preceding citizen science study, as compared with previous published distributions, was confirmed. This shift was also predicted by Maxent species distribution models, reflecting the broader distribution of the tick occurrence data contributed by citizens. Most D. reticulatus ticks were found on dogs (1,311/1,960, 66.9%), while D. marginatus was mainly discovered on hoofed animals (197/621, 31.7%) and humans (182/621, 29.3%). Human tick bites were reported in 0.7% (14/1,960) of host-assigned D. reticulatus and 3.4% (21/621) of host-assigned D. marginatus. Further studies to investigate an increasing endemisation of Babesia canis in Germany as well as the relevance of D. reticulatus for TBEV spread throughout the country, e.g., by traveling dogs, are urgently needed. In view of the activity of D. reticulatus during winter or the colder months, which complements that of Ixodes ricinus, a year-round tick protection of at least dogs is strongly recommended.
... Since then, D. reticulatus has increased its geographic range in Germany considerably (Földvári et al., 2016) and is still continuing to do so (Drehmann et al., 2020). This expansion is thought to be driven by factors including climate change, changed land use and increased abundance of hosts such as red foxes, wild boars and roe deer (Földvári et al., 2016). ...
... Since then, several endemic foci of babesiosis have been found in southern and southwestern areas of Germany (Beelitz et al., 2012). In a retrospective study, clusters of autochthonous infections were reported in Breisgau (Beelitz et al., 2008) in southern Germany, while only isolated cases occurred in the surrounding regions (Rubel et al., 2016;Drehmann et al., 2020). Furthermore, autochthonous infections with B. canis have been observed in dogs from Saarland (Beelitz et al., 2012), Baden-Württemberg (Barutzki et al., 2007) and ...
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Canine babesiosis caused by Babesia canis (Piana & Galli-Valerio, 1895) is emerging in new regions in Europe since its vector Dermacentor reticulatus (Fabricius, 1794) is expanding its geographic range. In the Berlin/Brandenburg area in northeast Germany, D. reticulatus is highly abundant but in the past only one autochthonous B. canis infection was reported. Since 2015, autochthonous cases were occasionally diagnosed but numbers increased since autumn 2019. The aim of the study was to genotype autochthonous canine Babesia spp. infections from Berlin/Brandenburg. Between 04/2015 and 01/2022, 46 dogs with acute babesiosis were presented to the small animal clinic (one dog was infected twice resulting in 47 samples). There were 32 dogs that had never left Berlin/Brandenburg and 14 others that had not left the region in the 6 weeks prior to disease onset. PCRs targeting the 18S rRNA and the Bc28.1 merozoite surface antigen were positive in 47 and 42 samples, respectively. Sequencing of cloned PCR products identified all samples as B. canis with 17 18S rRNA and 12 Bc28.1 haplotypes. Based on network analysis for 18S rRNA sequences and a previously described polymorphic dinucleotide, samples were assigned to two distinct clusters. One contained 31 and the other 16 samples. Using network analysis, the Bc28.1 haplotypes could also be separated into two clusters differing by at least five polymorphisms. Analyses of sequences from multiple clones indicated the presence of up to five 18S rRNA and eight Bc28.1 haplotypes and thus high parasite variability in an individual host. The genetic diversity could suggest that the parasites in the region have multiple origins, but diversity in individual dogs and dog populations from endemic regions is unknown. The suitability of both markers for genotyping is questionable due to potential intragenomic diversity for the rRNA and high intergenomic variability for the Bc28.1 marker.
... Such changes are the result of a complex interaction of factors, particularly increases in tick abundance and distribution driven by climatic factors allied to changes in land-use, habitat management and wild host abundance. Changes in tick-borne pathogen prevalence is of particular concern in the UK, since it sits at the northern edge of the range of one of the key vectors, D. reticulatusa tick that has seen rapid expansion of its range in mainland Europe (Drehmann et al., 2020). ...
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The emergence of Babesia pathogens novel to the UK is of growing concern; these include Babesia canis and Babesia caballi. However, a better understanding of changes in the prevalence of endemic Babesia species such as Babesia venatorum and Babesia divergens is also of importance. Here, the prevalence of Babesia pathogens in both Dermacentor reticulatus and Ixodes ricinus ticks was assessed. Dermacentor reticulatus were collected from six sites known to harbour populations of this species in west Wales and southern England. DNA was extracted from 879 individual ticks and subjected to PCR and sequence analysis. Seven Babesia species were detected in 7.5% of the ticks, including B. caballi (0.68%), B. bovis (1.7%), B. microti (1.02%), B. bigemina (0.34%), B. capreoli (0.34%), and one isolate of B. canis (0.34%). Two of the field sites with grazing equines present had ticks that were positive for B. caballi. For I. ricinus, up to 200 nymphs were collected from each of 24 cattle farms in south-west England. Nymphs were divided into 6 pools of 30 from each farm for DNA extraction, PCR, and sequencing. Samples from seven out of the 24 farms tested positive for Babesia, and most were positive for more than one species. Babesia divergens was identified from five farms, and three of these farms had two pooled samples positive for B. divergens, which given the low overall prevalence rate suggests that B. divergens may be highly clustered within the tick population. Most of the remaining positive samples were Babesia venatorum, demonstrating that this zoonotic pathogen is widespread in livestock habitats. The data suggest that B. canis is not yet widely prevalent in established D. reticulatus populations in the UK, but that there is a need to raise awareness of the risk of equine piroplasmosis in areas with endemic D. reticulatus foci, since B. caballi appears more widely established.
... The endemic area of B. canis has expanded from central Europe to the Baltic region, and new endemic foci of canine babesiosis have been documented in Germany, Poland, Lithuania and Latvia [6][7][8][9]. The spread of B. canis to new areas is closely connected to the expansion of the range of its main vector, the Dermacentor reticulatus tick [10][11][12]. In the last decade, D. reticulatus has expanded its range in Baltic countries. ...
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Canine babesiosis is an emerging and rapidly expanding tick-borne disease in central and northeast Europe. In the last two decades, the endemic area of Babesia canis has expanded from central Europe to the Baltic region. This study aimed to investigate the genetic diversity of B. canis strains isolated from naturally infected dogs in different regions of Lithuania using PCR-RFLP and sequence analyses based on a partial region of 18S rRNA and Bc28.1 genes. Blood samples from 149 dogs suspected of having babesiosis were collected in Lithuania during 2016–2017. Based on PCR-RFLP profiles and two nucleotide substitutions observed in 18S rRNA gene sequences, three B. canis genotypes were identified in Lithuania—18S rRNA-A, 18S rRNA-B and 18S rRNA-A/B—with the A/B genotype predominating (83.9%). Based on the obtained PCR-RFLP profiles of the Bc28.1 gene, four B. canis genotypes were identified: Bc28.1-B (53.8%), Bc28.1-34 (20.8%), Bc28.1-A (17.9%), and Bc28.1-34/A or B (7.5%). Sequence analysis of the partial Bc28.1 gene revealed eighteen polymorphic sites and thirteen sequence variants among the Lithuanian samples. The B. canis genotypes obtained were detected with varying prevalences in different regions of Lithuania.
... Its immature life stages (larvae and nymphs) parasitize mostly small mammals and birds. The second most common tick species in temperate Europe is the ornate cow tick, Dermacentor reticulatus, whose juvenile developmental stages feed mostly on small mammals [2,3]. Therefore, small mammals, predominantly rodents, are essential for the maintenance and distribution of ticks and tick-borne pathogens [4,5]. ...
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Background: Ixodid ticks are important vectors for zoonotic pathogens, with Ixodes ricinus being the most important in Europe. Rodents are hosts of immature life stages of I. ricinus ticks and are considered main reservoirs for tick-borne pathogens, e.g. Borrelia burgdorferi. The aim of this study was to analyse the prevalence as well as genospecies and sequence type (ST) diversity of Borrelia burgdorferi sensu lato in ticks and small mammals from central Germany and to elaborate on the influence of environmental and/or individual host and vector factors on Borrelia prevalence. Methods: After species identification, 1167 small mammal skin samples and 1094 ticks from vegetation were screened by B. burgdorferi sensu lato real-time polymerase chain reaction, and positive samples were characterized by multilocus sequence typing. Generalized linear (mixed) models were used to estimate how seasonality, small mammal species/tick life stage and habitat affect individual infection status. Results: In total, 10 small mammal species and three tick species, Ixodes ricinus, Ixodes inopinatus (both considered members of the I. ricinus complex) and Dermacentor reticulatus, were investigated. Borrelia DNA was detected in eight host species, i.e. the striped field mouse (Apodemus agrarius), the yellow-necked field mouse (Apodemus flavicollis), the wood mouse (Apodemus sylvaticus), the water vole (Arvicola amphibius), the bank vole (Clethrionomys glareolus), the field vole (Microtus agrestis), the common vole (Microtus arvalis), and the common shrew (Sorex araneus). Two species were Borrelia negative, the greater white-toothed shrew (Crocidura russula) and the pygmy shrew (Sorex minutus). The average prevalence was 6.2%, with two genospecies detected, Borrelia afzelii and Borrelia garinii, and at least three STs that had not been previously reported in small mammals. Borrelia prevalence in small mammals did not differ between seasons. Six genospecies of Borrelia—Borrelia afzelii, Borrelia valaisiana, Borrelia garinii, Borrelia lusitaniae, Borrelia spielmanii, and Borrelia burgdorferi sensu stricto—and 25 STs of Borrelia, of which 12 have not been previously described at all and five have not been previously reported in Germany, were detected in 13% of I. ricinus complex ticks. Prevalence was highest in adult females (25.3%) and lowest in nymphs (11.4%). Prevalence was significantly higher in ticks from grassland (16.8%) compared to forests (11.4%). Conclusions: The high level of small mammal diversity in this region of Germany seems to be reflected in a wide variety of genospecies and STs of B. burgdorferi.
... Another example is Rhipicephalus sanguineus (vector for multiple CVBDs), which is being introduced to non-endemic countries (i.e. Germany and Poland) and can establish temporary or permanent populations associated with human habitation or in the environment [12,17,[25][26][27][28][29]. Increased D. immitis infections have been caused by range expansion of both native mosquitos and imported Aedes species, climatic changes, and importation of dogs from endemic areas [4,5,10,11,30]. ...
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Background Canine vector-borne disease (CVBD) has been an area of increasing interest in Europe over the last few decades, and there have been changes in the prevalence and distribution of many of these diseases. Monitoring CVBD infections in Europe is often done by individual countries, but aggregated data for the European countries are helpful to understand the distribution of CVBDs. Methods We used an extensive retrospective database of results from point-of-care rapid enzyme-linked immunosorbent assay (ELISA) tests on dogs across Europe to identify distribution and seropositivity in animals tested for selected CVBDs ( Anaplasma spp. , Ehrlichia spp. , Borrelia burgdorferi, Leishmania spp., and Dirofilaria immitis ) from 2016 through 2020. Geographic distribution of positive tests and relative percent positive values were mapped by the Nomenclature of Territorial Units for Statistics classification for regions with sufficient test results for reporting. Results A total of 404,617 samples corresponding to 1,134,648 canine results were available from dogs tested in 35 countries over the 5-year study period. Over this period the number of test results per year increased whereas test positivity decreased. Leishmania spp. had the largest increase in total test results from 25,000 results in 2016 to over 60,000 results in 2020. Test positivity for Leishmania spp. fell from 13.9% in 2016 to 9.4% in 2020. Test positivity fell for Anaplasma spp. (7.3 to 5.3%), Ehrlichia spp. (4.3 to 3.4%), and Borrelia burgdorferi (3.3 to 2.4%). Dirofilaria immitis test positivity trended down with a high of 2.7% in 2016 and low of 1.8% in 2018. Leishmania spp. test positivity was highest in endemic areas and in several non-endemic countries with low numbers of test results. Co-positivity rates were significantly higher than expected for all pathogen test positive pairs except for Ehrlichia spp. with Borrelia burgdorferi and D. immitis with Borrelia burgdorferi . Conclusions This study represents the largest data set on CVBD seropositivity in Europe to date. The increase in the number of test results and decreasing test positivity over the study period may reflect changes in testing behavior and increased screening of healthy animals. The Europe-wide mapping of CVBD provides expected test positivity that can help inform veterinarians’ decisions on screening and improve prevention and identification of these important, sometimes zoonotic, diseases. Graphical Abstract
... In contrast, D. marginatus is assumed to be cold-sensitive, showing a high mortality at − 15 °C within a short period of time in the laboratory (Dörr and Gothe 2001). This is consistent with its distribution and occurrence records ranging furthest south among the three tick species (Drehmann et al. 2020). Under field conditions, ticks generally search for protected places to spend their diapause over the winter, which allows them to survive even in areas where temperatures fall below the survival thresholds identified under laboratory conditions. ...
Article
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Tick-borne diseases are a major health problem worldwide and could become even more important in Europe in the future. Due to changing climatic conditions, ticks are assumed to be able to expand their ranges in Europe towards higher latitudes and altitudes, which could result in an increased occurrence of tick-borne diseases. There is a great interest to identify potential (new) areas of distribution of vector species in order to assess the future infection risk with vector-borne diseases, improve surveillance, to develop more targeted monitoring program, and, if required, control measures. Based on an ecological niche modelling approach we project the climatic suitability for the three tick species Ixodes ricinus , Dermacentor reticulatus and Dermacentor marginatus under current and future climatic conditions in Europe. These common tick species also feed on humans and livestock and are vector competent for a number of pathogens. For niche modelling, we used a comprehensive occurrence data set based on several databases and publications and six bioclimatic variables in a maximum entropy approach. For projections, we used the most recent IPCC data on current and future climatic conditions including four different scenarios of socio-economic developments. Our models clearly support the assumption that the three tick species will benefit from climate change with projected range expansions towards north-eastern Europe and wide areas in central Europe with projected potential co-occurrence. A higher tick biodiversity and locally higher abundances might increase the risk of tick-borne diseases, although other factors such as pathogen prevalence and host abundances are also important.
... Importantly, the scheme provides information back to anyone submitting samples, promotes One Health responses to unusual findings and disseminates this information across government departments. Across Europe, this approach has been used to map the presence and expansion of tick populations, identify hot-spots for tick-human interactions and generate samples for pathogen testing [53][54][55][56]. ...
Article
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Where ticks are found, tick-borne diseases can present a threat to human and animal health. The aetiology of many of these important diseases, including Lyme disease, bovine babesiosis, tick-borne fever and louping ill, have been known for decades whilst others have only recently been documented in the United Kingdom (UK). Further threats such as the importation of exotic ticks through human activity or bird migration, combined with changes to either the habitat or climate could increase the risk of tick-borne disease persistence and transmission. Prevention of tick-borne diseases for the human population and animals (both livestock and companion) is dependent on a thorough understanding of where and when pathogen transmission occurs. This information can only be gained through surveillance that seeks to identify where tick populations are distributed, which pathogens are present within those populations, and the periods of the year when ticks are active. To achieve this, a variety of approaches can be applied to enhance knowledge utilising a diverse range of stakeholders (public health professionals and veterinarians through to citizen scientists). Without this information, the application of mitigation strategies to reduce pathogen transmission and impact is compromised and the ability to monitor the effects of climate change or landscape modification on the risk of tick-borne disease is more challenging. However, as with many public and animal health interventions, there needs to be a cost-benefit assessment on the most appropriate intervention applied. This review will assess the challenges of tick-borne diseases in the UK and argue for a cross-disciplinary approach to their surveillance and control.
Article
Objective: Canine babesiosis, an infectious disease transmitted by Dermacentor reticulatus, is exhibiting growing importance in Germany. The aim of this study was to display the increased incidence of canine babesiosis in the Rhine-Main area in Hesse, with special focus on the accumulation in the district of Groß-Gerau. Material and methods: The retrospective study included dogs presented to the veterinary hospital between October 2018 and December 2020 and diagnosed with canine babesiosis on the basis of a positive Babesia spp.-PCR. Results: A total of 697 dogs were tested by Babesia spp.-PCR during this time period. Of these, 81 (12 %) were positive.Sequencing was performed in 14 of the 81 dogs (17 %) (B. canis n = 13, B, vulpes n = 1). A simultaneous anaplasmosis infection was detected in 2 dogs. Strikingly, babesiosis cases occurred throughout the year with accumulations in March/April as well as in October.Evaluation of a complete blood cell count revealed pancytopenia in 44 of the 81 animals (54 %). Anemia was present in 66 (82 %), thrombocytopenia in 76 of the 81 patients (94 %). Only 2 of the 81 positive cases showed no hematological changes. Hyperbilirubinemia was found in 66 of 73 measured bilirubin levels (90 %).All animals were treated with two injections of imidocarb-diproprionate (Carbesia®) in 14-day intervals. Follow-up PCR was performed in 37 of the 81 patients (46 %). In the majority of cases (92 %), successful therapy was confirmed by a negative Babesia-PCR. A total of 6 of the 81 patients (7 %) were euthanized during the treatment period. The reasons for euthanasia were progressive renal disease, high-grade intravascular hemolysis necessitating multiple blood transfusions, and development of splenic and renal abscesses. Conclusion: In dogs with clinical signs such as apathy, pyrexia and hemoglobinuria, as well as hematologic abnormalities comprising anemia, thrombocytopenia as well as pancytopenia, babesiosis needs to be included in the list of differential diagnoses. Testing should be initiated accordingly regardless of the season, however especially in spring and autumn.
Thesis
In the last decades, the emergence of ticks and tick-borne diseases (TBD) has become a public health concern in Europe. In Piedmont region (Northwestern Italy) ticks were rare in the past, especially in mountain areas. However, in the recent years, we have been observing an increase in tick abundance in the environment but also in reported tick-bites and TBD cases in humans. Tick-borne diseases are characterized by complex transmission cycles; thus, an integrated approach is needed. The ‘One Health’ (OH) approach may effectively provide scientific evidence for TBD surveillance and prevention, and support decision makers. This PhD project investigates the presence and abundance of tick vectors and tick-borne pathogens in two natural areas of Piedmont region, recently invaded by ticks, to identify potential risk factors involved in their emergence, and to evaluate their impact on public health. Additionally, we aimed to identify ideal surveillance and control elements based on a OH approach. We recorded a further expansion of Ixodes ricinus in Europe, being maintained at altitudes up to around 1700 m a.s.l. The abundance of I. ricinus was significantly associated with altitude, habitat type and signs of roe deer presence and molecular analyses demonstrated its infection with several zoonotic agents: B. burgdorferi sensu lato, spotted fever group rickettsiae, Anaplasma phagocytophilum, Borrelia miyamotoi and Neoehrlichia mikurensis. Dermacentor spp. ticks were also collected, in particular D. marginatus and D. reticulatus. Rickettsia slovaca and Candidatus Rickettsia rioja, causative agents of SENLAT (Scalp Eschar Neck Lymphadenopathy) syndrome in humans, infected Dermacentor ticks and wild boar tissues, suggesting the greater contribution of wild boar in its eco-epidemiology and dispersion in the study area. We also confirmed that Piedmontese population is exposed to infected tick bites. However, a generalized low awareness was observed among the population; in fact, although most citizens perceive ticks as a health threat, they do not frequently adopt protective measures. This justified the longer duration of tick attachment generally observed in bitten patients (> 24 hours). A serosurvey in wild ungulates was additionally carried out in mountain areas to assess the circulation of tick-borne encephalitis virus. No serum sample yielded positive results, indicating the absence of this pathogen in our territory so far. Notwithstanding, this activity should be maintained in the long term for early pathogen detection and rapid response, since the virus is circulating in bordering areas of the Piedmont. Regarding tick ecology, this project integrated some investigations about tick symbionts, whose presence is key for tick development and survival. We detected the infection of Francisella-like endosymbionts in Dermacentor spp. which have been previously associated with positive effects in the tick fitness, by providing nutrimental support to ticks. Moreover, a large-scale study was carried out to investigate the infection of Rickettsiella symbionts in I. ricinus populations in Europe, identifying a great diversity within the Rickettsiella genus. Research on TBD requires the knowledge and skills from different disciplines. However, transdisciplinarity seems to work when structural support is provided by the system; instead, critical elements such as insufficient funding, system decentralization and monodisciplinary approaches threaten the response capacity of the systems. One Health operation and infrastructure aspects can strengthen surveillance systems and could be particularly important in areas of recent spread of ticks and TBD.
Article
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Background: Tick-borne encephalitis (TBE) is the most common viral CNS infection with incidences much higher than all other virus infections together in many risk areas of central and eastern Europe. The Odenwald Hill region (OWH) in southwestern Germany is classified as a TBE risk region and frequent case numbers but also more severe infections have been reported within the past decade. The objective of the present study was to survey the prevalence of tick-borne encephalitis virus (TBEV) in Ixodes ricinus and to associate TBEV genetic findings with TBE infections in the OWH. Methods: Ticks were collected by the flagging methods supported by a crowdsourcing project implementing the interested public as collectors to cover completely and collect randomly a 3532 km2 area of the OWH TBE risk region. Prevalence of TBEV in I. ricinus was analysed by reversed transcription quantitative real-time PCR. Phylogeographic analysis was performed to classify OWH TBEV isolates within a European network of known TBEV strains. Mutational sequence analysis including 3D modelling of envelope protein pE was performed and based on a clinical database, a spatial association of TBE case frequency and severity was undertaken. Results: Using the crowd sourcing approach we could analyse a total of 17,893 ticks. The prevalence of TBEV in I. ricinus in the OWH varied, depending on analysed districts from 0.12% to 0% (mean 0.04%). Calculated minimum infection rate (MIR) was one decimal power higher. All TBEV isolates belonged to the European subtype. Sequence analysis revealed a discontinuous segregation pattern of OWH isolates with two putative different lineages and a spatial association of two isolates with increased TBE case numbers as well as exceptional severe to fatal infection courses. Conclusions: TBEV prevalence within the OWH risk regions is comparatively low which is probably due to our methodological approach and may more likely reflect prevalence of natural TBEV foci. As for other European regions, TBEV genetics show a discontinuous phylogeny indicating among others an association with bird migration. Mutations within the pE gene are associated with more frequent, severe and fatal TBE infections in the OWH risk region.
Article
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Tick-borne encephalitis virus (TBEV; family Flaviviridae) is the most medically important tick-borne virus in Europe and Asia. Ixodes ricinus and I. persulcatus ticks are considered to be the main vector ticks of TBEV in nature due to their specific ecological associations with the vertebrate hosts. Nevertheless, recent TBEV prevalence studies in ticks suggest that Dermacentor reticulatus ticks might play a relevant role in the maintenance of TBEV in nature. The goal of this study was to evaluate the vector competency of D. reticulatus for TBEV through experimental tick infections and comparative in vivo transmission studies involving D. reticulatus and I. ricinus ticks. We observed that after a transcoxal micro-capillary inoculation, adult female D. reticulatus ticks efficiently replicated TBEV during the observed period of 21 days. The mean virus load reached up to 2.5 × 10⁵ gene copies and 6.4 × 10⁴ plaque forming units per tick. The infected D. reticulatus ticks were able to transmit the virus to mice. The course of infection in mice was comparable to the infection after a tick bite by I. ricinus while the virus spread and clearance was slightly faster. Moreover, D. reticulatus ticks were capable of tick-to-tick non-viraemic transmission of TBEV to the Haemaphysalis inermis nymphs during co-feeding on the same animal. The co-feeding transmission efficiency was overall slightly lower (up to 54%) in comparison with I. ricinus (up to 94%) and peaked 1 day later, at day 3. In conclusion, our study demonstrated that D. reticulatus is a biologically effective vector of TBEV. In line with the recent reports of its high TBEV prevalence in nature, our data indicate that in some endemic foci, D. reticulatus might be an underrecognized TBEV vector which contributes to the expansion of the TBEV endemic areas.
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Background: The bacterium Coxiella burnetii is the etiological agent of Q fever and is mainly transmitted via inhalation of infectious aerosols. DNA of C. burnetii is frequently detected in ticks, but the role of ticks as vectors in the epidemiology of this agent is still controversial. In this study, Ixodes ricinus and Dermacentor marginatus adults as well as I. ricinus nymphs were fed on blood spiked with C. burnetii in order to study the fate of the bacterium within putative tick vectors. Methods: Blood-feeding experiments were performed in vitro in silicone-membrane based feeding units. The uptake, fecal excretion and transstadial transmission of C. burnetii was examined by quantitative real-time PCR as well as cultivation of feces and crushed tick filtrates in L-929 mouse fibroblast cells and cell-free culture medium. Results: Ticks successfully fed in the feeding system with engorgement rates ranging from 29% (D. marginatus) to 64% (I. ricinus adults). Coxiella burnetii DNA was detected in the feces of both tick species during and after feeding on blood containing 105 or 106 genomic equivalents per ml blood (GE/ml), but not when fed on blood containing only 104 GE/ml. Isolation and cultivation demonstrated the infectivity of C. burnetii in shed feces. In 25% of the I. ricinus nymphs feeding on inoculated blood, a transstadial transmission to the adult stage was detected. Females that molted from nymphs fed on inoculated blood excreted C. burnetii of up to 106 genomic equivalents per mg of feces. Conclusions: These findings show that transstadial transmission of C. burnetii occurs in I. ricinus and confirm that I. ricinus is a potential vector for Q fever. Transmission from both tick species might occur by inhalation of feces containing high amounts of viable C. burnetii rather than via tick bites.
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Background: Tick-borne encephalitis (TBE) virus is transmitted to humans and animals through tick bites and is thought to circulate in very strictly defined natural environments called natural foci. The most common tick serving as a vector for the TBE virus in central Europe is Ixodes ricinus; it is rarely found in other tick species and in Dermacentor reticulatus it has, so far, only been reported in Poland. Methods: Between autumn 2016 and spring 2018 ticks were collected by the flagging method in a new TBE focus in the district of northern Saxony, Germany, outside the known risk areas as defined by the national Robert Koch Institute. Ticks were morphologically identified and tested in pools for the presence of TBE virus using a real-time RT-PCR. TBE virus from positive pools was isolated in A549 cells, and the E gene sequences were determined after conventional RT-PCR, followed by a phylogenetic comparison. Results: TBE virus was detected in 11 pools, 9 times in flagged adults D. reticulatus (n = 1534; MIR: 0.59%, CI: 0.29– 11.3%) and only twice in I. ricinus nymphs (n = 349; MIR: 0.57%, CI: 0.02–2.2%). All other ticks, I. ricinus males (n = 33), females (n = 30) and larvae (n = 58), as well as 5 I. inopinatus (2 females, 3 males) and 14 Haemaphysalis concinna (3 females, 11 nymphs), tested negative for TBE virus. TBE virus was not detected in I. ricinus during the summer, when D. reticulatus is not active. Sequence comparison of the entire E gene of the isolated virus strains resembled each other with only 3 nucleotide differences. The most closely related viral sequences belong to TBE virus strains from Poland and Neustadt an der Waldnaab (county of Neustadt an der Waldnaab, Bavaria), approximately 200 km east and 200 km south-west of the new focus, respectively. Conclusions: TBE virus was found in northern Saxony, Germany, with similar MIRs in D. reticulatus and I. ricinus, indicating that D. reticulatus plays an equal role to I. ricinus in virus circulation when both tick species are sympatric.
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Understanding and responding to the ecological, social and economic conditions that facilitate disease emergence and transmission represents a substantial challenge for epidemiologists and health professionals. In this article we integrate knowledge about the human and the vector population, to provide a context from which to examine the underlying causal factors of D. marginatus-borne diseases emergence in the study area. Within this framework we analyse the biotic and abiotic factors that drive D. marginatus population dynamics and the role of its typical host for dispersal. These investigations suggest that D. marginatus is a tick species prone to spatially overlap its presence with human population presence. Then we consider the public health implications for the residents, when simply carrying out trivial outdoor activities may increase the risk to contact an infected tick.
Article
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Lyme disease is the most common tick-borne disease in North America and Europe, and on-going surveillance is required to monitor the spread of the tick vectors as their populations expand under the influence of climate change. Active surveillance involves teams of researchers collecting ticks from field locations with the potential to be sites of establishing tick populations. This process is labor- and time-intensive, limiting the number of sites monitored and the frequency of monitoring. Citizen science initiatives are ideally suited to address this logistical problem and generate high-density and complex data from sites of community importance. In 2014, the same region was monitored by academic researchers, public health workers, and citizen scientists, allowing a comparison of the strengths and weaknesses of each type of surveillance effort. Four community members persisted with tick collections over several years, collectively recovering several hundred ticks. Although deviations from standard surveillance protocols and the choice of tick surveillance sites makes the incorporation of community-generated data into conventional surveillance analyses more complex, this citizen science data remains useful in providing high-density longitudinal tick surveillance of a small area in which detailed ecological observations can be made. Most importantly, partnership between community members and researchers has proven a powerful tool in educating communities about of the risk of tick-vectored diseases and in encouraging tick bite prevention.
Article
Dermacentor reticulatus is one of the most important European tick species. However, its spatial distribution, seasonality and regional vector role are not well known. This study aimed to gather information about abundance patterns of questing ticks and associated pathogens in unfed female adult D. reticulatus in the Berlin/Brandenburg area. Using the flagging method, questing ticks were collected at four sites in 2010–2012 and 2000 D. reticulatus were analysed regarding infection with Rickettsia, Babesia, Borrelia and Anaplasmataceae by conventional or real-time PCR. Dermacentor reticulatus showed a bimodal activity pattern: highest numbers of adult ticks were recorded between March and end of May (mean 50 ticks/h) and from mid-August until end of November (mean 102 ticks/h). During summer, almost complete inactivity was observed (mean 0.4 ticks/h). Sporadic samplings from December to February revealed tick activity also during winter (mean 47 ticks/h), which was characterised by large fluctuations. Using negative binomial regression analysis, significant influences of the variables sampling site, season and temperature on the abundance of questing D. reticulatus were determined. The parameters relative humidity and year were not of significant importance. PCR analyses showed an average prevalence of 64% for Rickettsia sp. Large differences in pathogen frequencies were observed between sampling sites (31.4–78.3%). Regression analysis demonstrated a significant influence of the sampling site but not of season and year. Examinations regarding other pathogen groups indicated prevalences of 0.25% (Borrelia sp.) and 0.05% (Anaplasmataceae) but absence of Babesia sp. Sequencing of positive samples revealed infections with Rickettsia raoultii, Borrelia miyamotoi, Borrelia afzelii and Anaplasma phagocytophilum. The study shows stable populations of D. reticulatus in Berlin/Brandenburg. People should be aware of ticks throughout the year since Ixodes ricinus is co-endemic and active in spring, summer and autumn while adult D. reticulatus are active throughout the year and even in winter during periods of frost as long as it is warming up during the day. Prevalence of R. raoultii in the present study is among the highest described for D. reticulatus. Borrelia miyamotoi was detected for the first time in D. reticulatus, illustrating the importance of screening studies to evaluate the pathogen structure in D. reticulatus populations.
Article
Babesiosis, caused by piroplasmid protozoans in the genus Babesia, is arguably the most important vector-borne disease of livestock and companion animals and is growing in importance as a zoonosis. Ixodid ticks were identified as vectors more than a hundred years ago, but the particular tick species transmitting some significant pathogens are still unknown. Moreover, it is only recently that the complexity of the pathogen-tick relationship has been revealed as a result of studies enabled by gene expression and RNA interference methodology. In this article, we provide details of demonstrated and incriminated vectors, maps of the current knowledge of vector distribution, a summary of established features of the pathogen life cycle in the vector, and an outline of molecular research on pathogen-tick relationships. The article concludes with a discussion of vector ecology and disease epidemiology in a global-change context and with suggestions for future research. Expected final online publication date for the Annual Review of Entomology Volume 64 is January 7, 2019. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
Book
This book includes descriptive keys for identifying every stage of all the species of ticks reported in Europe and northern Africa. It includes descriptive texts on the ecology and prominent features of each species, together with ink illustrations and distribution maps of more than 60 species of hard and soft ticks. The text for each species was prepared by specialists, the illustrations were made especially for this book and the maps were compiled on the basis of more than 40 years of records. This book is the first to offer keys for more than 60 species of ticks (both immature and adult) in the target territory. It also includes supplementary information with bibliographical details for each species. This book is based upon work from COST Action TD1303, supported by COST (European Cooperation in Science and Technology)