Invasive raccoon (Procyon lotor) and raccoon dog (Nyctereutes procyonoides) as potential reservoirs of tick-borne pathogens: data review from native and introduced areas

Abstract

In recent decades, populations of the raccoon ( Procyon lotor ) and the raccoon dog ( Nyctereutes procyonides ) have increased and adapted to peri-urban and urban environments in many parts of the world. Their ability to rapidly colonize new territories, high plasticity and behavioral adaptation has enabled these two species to be considered two of the most successful invasive alien species. One of the major threats arising from continually growing and expanding populations is their relevant role in maintaining and transmitting various vector-borne pathogens among wildlife, domestic animals and humans. According to the WHO, over 17% of infectious diseases are vector-borne diseases, including those transmitted by ticks. Every year tick-borne pathogens (TBPs) create new public health challenges. Some of the emerging diseases, such as Lyme borreliosis, anaplasmosis, ehrlichiosis, babesiosis and rickettsiosis, have been described in recent years as posing important threats to global health. In this review we summarize current molecular and serological data on the occurrence, diversity and prevalence of some of the TBPs, namely Babesia , Theileria , Hepatozoon , Borrelia , Rickettsia , Bartonella , Anaplasma and Ehrlichia , that have been detected in raccoons and raccoon dogs that inhabit their native habitats and introduced areas. We draw attention to the limited data currently available on these invasive carnivores as potential reservoirs of TBPs in different parts of the world. Simultaneously we indicate the need for more research in order to better understand the epidemiology of these TBPs and to assess the future risk originating from wildlife.
Graphical Abstract

Full text

Myśliwyetal. Parasites & Vectors (2022) 15:126
https://doi.org/10.1186/s13071-022-05245-3
REVIEW
Invasive raccoon (Procyon lotor) andraccoon
dog (Nyctereutes procyonoides) aspotential
reservoirs oftick-borne pathogens: data review
fromnative andintroduced areas
Izabella Myśliwy, Agnieszka Perec‑Matysiak and Joanna Hildebrand*
Abstract
In recent decades, populations of the raccoon (Procyon lotor) and the raccoon dog (Nyctereutes procyonides) have
increased and adapted to peri‑urban and urban environments in many parts of the world. Their ability to rapidly colo‑
nize new territories, high plasticity and behavioral adaptation has enabled these two species to be considered two of
the most successful invasive alien species. One of the major threats arising from continually growing and expanding
populations is their relevant role in maintaining and transmitting various vector‑borne pathogens among wildlife,
domestic animals and humans. According to the WHO, over 17% of infectious diseases are vector‑borne diseases,
including those transmitted by ticks. Every year tick‑borne pathogens (TBPs) create new public health challenges.
Some of the emerging diseases, such as Lyme borreliosis, anaplasmosis, ehrlichiosis, babesiosis and rickettsiosis, have
been described in recent years as posing important threats to global health. In this review we summarize current
molecular and serological data on the occurrence, diversity and prevalence of some of the TBPs, namely Babesia,
Theileria, Hepatozoon, Borrelia, Rickettsia, Bartonella, Anaplasma and Ehrlichia, that have been detected in raccoons and
raccoon dogs that inhabit their native habitats and introduced areas. We draw attention to the limited data currently
available on these invasive carnivores as potential reservoirs of TBPs in different parts of the world. Simultaneously we
indicate the need for more research in order to better understand the epidemiology of these TBPs and to assess the
future risk originating from wildlife.
Keywords: Invasive species, Raccoon dog, Nyctereutes procyonides, Raccoon, Procyon lotor, Tick‑borne pathogens,
Vector‑borne pathogens, Wildlife
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Background
Wildlife species undisputedly serve as prime reservoirs
of vector-borne pathogens. Invasive alien species in par-
ticular may play an important role in this context as they
provide pathogens with opportunities to increase their
abundance in the environment and spread their geo-
graphical and host range. In the future this may result
in the bidirectional transmission of pathogens between
wildlife and domestic animals [1–3]. is unrestricted
flow of new pathogens may also have an impact on
human health. In recent years, due to urbanization, cli-
mate change and the destruction of natural ecosystems,
the populations of many wildlife species have increased
and adapted to environments in close proximity to
human populations and domestic animals [4]. ere-
fore, investigations on the distribution of pathogens and
the dynamics of infections among wildlife and domestic
Open Access
Parasites & Vectors
*Correspondence: joanna.hildebrand@uwr.edu.pl
Department of Parasitology, Faculty of Biological Sciences, University
of Wrocław, Wrocław, Poland
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Myśliwyetal. Parasites & Vectors (2022) 15:126
animals are of great importance for a better understand-
ing of their epidemiology [4–6].
e raccoon (Procyon lotor) is a North American mem-
ber of the Procyonidae family and was introduced to
Europe in the 1930s for fur farming and hunting, and as
a pet [7, 8]. e species rapidly proliferated and spread
across Europe [9–13]. In Japan, the raccoon was first
introduced in the 1960s where, after the spectacular suc-
cess of the animated cartoon ‘Rascal raccoon’ in 1977, it
was imported from North America and popularized as
a pet [10, 14]. e raccoon is highly adaptable to vary-
ing environmental conditions and is a host to numerous
human pathogens, including the nematode Baylisascaris
procyonis that is a causative agent of a severe ocular and
neurological illness in many species of animals as well as
in humans [12, 15, 16]. It has been confirmed that this
mesocarnivore has synanthropic potential not only in
its native areas but also in territories where it has been
newly introduced [16–18].
e raccoon dog (Nyctereutes procyonoides) is a mem-
ber of the Canidae family and is native to eastern Asia.
ere are six distinguished subspecies: Nyctereutes pro-
cyonoides Gray, 1834; N. p. orestes omas, 1923; N. p.
koreensis Mori, 1922; N. p. ussuriensis Matschie, 1907;
N. p. viverrinus Temminck, 1838; and N. p. albus Beard,
1904. is invasive carnivore was introduced into Europe
for its fur in the middle of the twentieth century [19]. e
ability of the raccoon dog to adapt to various environ-
mental conditions and its high behavioral plasticity and
reproductive capacity are the prime factors driving its
colonizing success in Europe. ey are an important res-
ervoir of numerous zoonotic pathogens which may pose
a threat to public health as well as to the biodiversity of
native fauna. In addition to the red fox, in central Europe
the raccoon dog can also act as a definitive host for the
zoonotic parasite Echinococcus multilocularis, which
causes alveolar echinococcosis, considered to be one of
the most dangerous zoonoses [2, 20–22].
e increasing prevalence and transmission of tick-
borne diseases (TBDs) are major public health issues, as
over 17% of infectious diseases, including TBDs, are vec-
tor-borne. Borrelia spp., Anaplasma spp., Rickettsia spp.,
Ehrlichia spp. and Babesia spp. are emerging tick-borne
pathogens which are highly important in terms of ani-
mal and human health worldwide [23, 24]. Raccoons and
raccoon dogs have been shown to gradually spread their
geographical range and colonize non-native territories
and to be able to reach high population density within
a short time, thereby playing a significant role in patho-
gen circulation. Some studies have shown that species
introduced into a new environment often lose their own
parasites during the course of establishing a new popu-
lation (Enemy Release Hypothesis) [25] but that they
also encounter and accumulate parasites which occur
in the newly colonized areas. e very few publications
included in the analysis presented in this review refer to
both the raccoon and raccoon dog as introduced species
that serve as potential reservoirs of tick-borne patho-
gens outside their native habitat, particularly in Europe
where research has been focused principally on intestinal
microparasites and helminth identification [26–31].
e aim of this review was to provide an overview of
published data on raccoons and raccoon dogs as wildlife
reservoirs and possible sentinels for tick-borne patho-
gens of bacterial and parasitic origin in their native and
introduced habitats. Simultaneously, we indicate the
importance of and direction for future research based on
key gaps in current knowledge.
Data sources
Publications providing data on the tick-borne pathogens
reported in raccoons and raccoon dogs worldwide were
identified using search engines and the Web of Science,
Scopus and Google Scholar databases. e search results
were manually checked and verified individually. All of
the included articles were written in English and Japanese
and were published between 1972 and 2021 in scientific
journals. is review does not include abstracts from
conferences or dissertations.
Molecular andserological data
Raccoon (Procyon lotor)
Babesia spp./Theileria spp.
Several Babesia parasites have been confirmed to poten-
tially infect raccoons. Before molecular testing, the Babe-
sia species parasitizing raccoons was named B. lotori
based on microscopic observations [32]. In Japan, where
raccoons are a non-native species, molecular studies
confirmed Babesia sp. (from the Babesia sensu stricto
[s.s.] group), Babesia microti-like and also Babesia spe-
cies similar to B. lotori. e B. microti-like parasite was
reported in two raccoons from Hokkaido, Japan, and
despite the capture of 372 raccoons, only 24 were exam-
ined for the presence of this protozoan. All of the animals
selected for examination had a significant splenomegaly,
which is one of the clinical manifestations of babesiosis.
DNA sequences extracted from two blood samples col-
lected from raccoons testing positive for this protozoan
were found to be identical to those from the USA, based
on small subunit ribosomal DNA (SSU-rDNA) analysis,
leading to the conclusion that this pathogen might have
been introduced to Japan together with the raccoon from
North America [33–35]. In the studies undertaken by
Jinnai etal. [35], six out of 348 (1.7%) blood samples col-
lected from raccoons obtained from Hokkaido gave PCR-
positive signals for the presence of Babesia DNA. is
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Myśliwyetal. Parasites & Vectors (2022) 15:126
study identified, for the first time, five unknown parasites
belonging to the Babesia sp. from feral Japanese rac-
coons. Four sequences were classified into a novel group
within Babesia genus (Clade 1) and one sequence was
found to be classified into Clade 2 which also contained
Babesia sp. found in the ixodid tick from Japan as well
as Babesia sp., B. divergens and B. odocoilei reported in
raccoons from the USA. ese results indicated that new
Babesia parasites may have established a new life-cycle in
Japanese feral raccoons. Information provided by stud-
ies conducted in the USA confirmed that there are four
putative piroplasm species present in raccoons from the
USA (i.e. B. lotori, B. microti-like, a novel Babesia s.s. and
a novel western Babesia sp.) with an additional fifth spe-
cies found only in the Japanese population of raccoons
[36, 37]. Babesia microti-like was the most common piro-
plasm detected in raccoons from the USA. is parasite
was found for the first time in a raccoon from Massachu-
setts [38]. High prevalence has been reported in raccoons
from Florida (82.4%) and North Carolina (84%), Minne-
sota and Colorado (66%). e results of studies under-
taken by Garrett etal. [37] also showed high prevalence
(62%) of B. microti-like in raccoons sampled from various
locations in the USA and Canada. e survey conducted
by Modarelli etal. [39] revealed for the first time the pres-
ence of the B. microti in raccoons from Texas (33.3%),
with the reported sequence resembling one isolated
from raccoons in Florida and Northern USA. Addition-
ally, two different Babesia species have been detected:
Babesia sp. Coco and another Babesia spo. which most
closely resembles Babesia sp. AJB-1006 detected in a rac-
coon in Illinois [36, 37, 39–41]. Babesia lotori (previously
referred to as Babesia s.s. and Babesia sp. AJB-2006) has
been found in a single raccoon from Illinois that had
clinical symptoms, and in raccoons from Minnesota and
Colorado, North Carolina and various other states in the
USA [36, 37, 40, 42]. No data on potential tick vectors for
any Babesia spp. of raccoons in the USA and Japan are
currently available. Only a few individuals of European
raccoons in Austria and Spain have been tested for Babe-
sia sp., and none of these were found to be infected with
this protozoan [28, 43]. e nomenclature of the Babesia
species detected in raccoons is still inconsistent.
Hepatozoon spp.
e presence of Hepatozoon spp. in raccoons was dem-
onstrated by molecular methods in surveys carried out in
the USA [39, 44]. Hepatozoon canis was reported for the
first time in the European population of this carnivore in
Spain, with an overall prevalence of 2.6%. is study is
the first and the only study of this parasite infection in
raccoons from Europe [45].
Borrelia spp.
Most of the data on this spirochete in raccoons origi-
nates from the USA and is based on the results of sero-
logical testing [46–53]. Antibodies against Borrelia
burgdorferi, B. lonestari or B. turicatae were detected.
Yabsley etal. [50] attempted to confirm the seropositive
results by the PCR method; however, no Borrelia DNA
was detected during molecular testing. e molecu-
lar results from studies carried out by Tufts etal. [54]
show the presence of B. burgdorferi only in one out of
39 raccoons. e only study on this spirochetal infec-
tion in raccoons from introduced areas was conducted
in Japan, in which only one sample was seropositive for
both Borrelia afzelii (0.1%) and Borrelia garinii (0.1%)
[54, 55].
Rickettsia spp.
Most of the studies on the detection of Rickettsia in rac-
coons were conducted in the USA using serological
methods, resulting in the detection of Rickettsia rick-
ettsii, R. montana, R. parkeri and R. bellii 369-C strain.
e most frequently detected species was R. rickettsii,
which is an etiological agent of Rocky Mountain spotted
fever (RMSP) in North and South America [51, 52, 54,
56–61]. Molecular research carried out in Japan revealed
the presence of Rickettsia japonica, R. tsutsugamushi, R.
felis, R. heliongjiangensis/R. japonica, R. amblyommi, R.
helvetica and Rickettsia sp. Hj126 [55, 62, 63]; in these
studies, a high number of animals were tested (n = 699,
n = 752 and n = 194, respectively). Rickettsia japonica
is a causative agent of RMSF in Japan. All detected spe-
cies were found to be pathogenic to humans, with the
exception of Rickettsia sp. Hj126 whose pathogenicity is
unknown. European populations of raccoon have not yet
been examined.
Bartonella spp.
Little is known about infection by this pathogen in rac-
coons. e results of molecular research in the USA
demonstrated the presence of the DNA of Bartonella
rochalimae, B. henselae, B. koehlerae and B. berkhoffii in
samples collected from raccoons. e dominant detected
species was B. henselae, which is a causative agent of
cat-scratch disease in humans [64–67]. Researchers in
Canada were the first to identify lesions associated with
Bartonella infection in a raccoon. e species identified
in this animal was closely related to Bartonella taylorii
[68]. A study in Japan found no Bartonella species in 977
blood samples collected from raccoons [69]. ere is no
research data currently available on the occurrence of
Bartonella among raccoons introduced into Europe.
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Myśliwyetal. Parasites & Vectors (2022) 15:126
Anaplasma spp.
Molecular and serological methods have confirmed Ana-
plasma infection among raccoons from the USA, with
the results showing that raccoons may be infected with
Anaplasma phagocytophilum. However, in these stud-
ies, the seropositive results were not always confirmed
by PCR tests [50, 54, 70, 71]. In Japan, molecular studies
undertaken by Sashika etal. [72] confirmed for the first
time the presence of Aanaplasma bovis in blood from
raccoons, with pathogen DNA detected in 36 out of 699
examined samples; no DNA of A. phagocytophilum was
found during that study. ese results suggest that rac-
coons could be a potential reservoir for A. bovis. Another
study showed a seropositive reaction towards A. phagocy-
tophium in one raccoon sample, although PCR testing did
not confirm this result [73]. In Europe, a limited number
of molecular studies have been conducted, on raccoons
from Austria, Czech Republic, Germany and Poland [6,
28, 74]; however, A. phagocytophilum DNA was found
only in one raccoon that originated from Poland.
Ehrlichia spp. andCandidatus Neoehrlichia spp.
In the USA, the most commonly used methods to detect
Ehrlichia in raccoons have been serological methods.
Seropositive results were obtained for Ehrlichia canis and
Ehrlichia chaffeensis in a number of studies, but almost all
results were PCR negative with the exception of one sam-
ple that was seropositive for E. canis. Both E. canis and E.
chaffeensis are etiological agents of monocytic ehrlichio-
sis [50, 51, 54, 71, 75, 76]. A number of molecular stud-
ies have been carried out in Europe. Studies conducted
in Austria and Spain targeted the detection of E. canis,
which infects wild carnivores and domestic dogs world-
wide [28, 45]. In the Austrian study, only four individuals
were examined and no pathogen was detected. However,
in the Spanish study, 194 individuals were tested and the
prevalence of E. canis sp. DNA was 2.6%. DNA of Ehr-
lichia sp. was not detected in any of 15 raccoons exam-
ined from the Czech Republic [6] (see also [77]). Only
two studies have been performed to detect Ehrlichia in
Japanese raccoons [72, 73]. From the 187 animals exam-
ined by Inokuma etal. [73], only one and three raccoons
showed a serological reaction to E. canis and E. chaffeen-
sis, respectively, but PCR testing did not confirm these
results. A molecular survey undertaken by Sashika etal.
[72] showed no presence of either E. canis or E. chaffeen-
sis DNA in 699 tested animals. Candidatus Neoehrlichia
lotoris has been detected only in raccoons from the USA
in which its prevalence is quite high—53.3% [71] and 67%
[78]. It has been confirmed that this species is closely
related to Candidatus Neoehrlichia mikurensis, and it
was originally named as a novel Ehrlichia-like organism
based on 16S rRNA gene sequence. As a result, the rac-
coon is considered to be a natural host of Candidatus
Neoehrlichia lotoris [71, 78, 79]. Surveys from Poland,
Germany and the Czech Republic did not show any pres-
ence of Candidatus Neoehrlichia sp. DNA in the exam-
ined samples [6, 74].
A detailed summary of currently available data on tick-
borne pathogens (TPBs) in the raccoon is provided in
Table1.
Raccoon dog (Nyctereutes procyonides)
Babesia spp./Theileria spp.
e first molecular report of B. microti-like in wild rac-
coon dogs in South Korea indicated that these canids may
play an important role as a source of piroplasm infection
for both domestic dogs and humans [80]. However, in
a study undertaken several years later in South Korea,
Hong etal. [81] did not confirm any B. microti-like PCR-
positive samples originating from 23 raccoon dogs. Stud-
ies on eileria spp. have been conducted only in South
Korea, and did not show the presence of this protozoan
in the examined blood samples from raccoon dogs [82].
In Europe, the results of research conducted by Duscher
etal. [28] were the first confirmation of B. microti-like in
an introduced population of raccoon dogs.
Hepatozoon spp.
To date there have been no studies conducted on the
detection of Hepatozoon spp. in raccoon dogs in either
native or introduced areas.
Borrelia spp.
A study in South Korea using molecular techniques
resulted in the first report of B. theileri in raccoon dogs
[83]. is study also identified Haemaphysalis flava, a
dominant species of a tick that infests raccoon dogs in
South Korea. e results of this survey indicated that
B. theileri can infect not only ungulate species but also
canine species, such as raccoon dogs. Further studies are
needed to define the role of this carnivore as a potential
reservoir of B. theileri [22]. Molecular studies under-
taken by Wodecka etal. [84] on European raccoon dogs
in western Poland revealed that eight out of 28 tested
animals were positive for Borrelia sp., with the domi-
nant species being B. garinii, followed by less prevalent
B. afezelii and B. valaisiana. is study indicated that
the role of raccoon dogs as a potential reservoir for the
bird-adapted B. garnii should be thoroughly investigated.
Additionally, in this same study, Borrelia species were
identified in 20.1% of ixodid ticks collected from the rac-
coon dogs examined [84].
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Table 1 Tick‑borne pathogens of parasitic and bacterial origin detected in raccoon (Procyon lotor) in its native and introduced range
TBPs Species/genospecies Locality Prevalence Diagnostic test References
Babesia/Theileria spp. B. microti‑like USA‑native 1/1 (100%) PCR [38]
B. microti‑like Japan‑introduced 2/24 (8.3%) PCR [34]
Babesia sp. USA‑native 1/1 (100%) PCR [42]
B. microti‑like USA‑native 34/41 (84%) PCR [40]
Babesia sp. 37/41 (90%)
Babesia sp.Japan‑introduced 6/348 (1.7%) PCR [35]
Theileria sp. 0/348
B. microti‑like 0/348
B. microti‑like USA‑native 14/17 (82.4%) PCR [41]
B. microti‑likeaAustria‑introduced 0/4 PCR [28]
B. microti‑like USA‑native 70/106 (66%) PCR [36]
Babesia sp. 11/106 (10%)
B. microti‑like USA/Canada 490/699 (70%) PCR [37]
Babesia sp.170/699 (24%)
B. microti USA‑native 5/15(33.3%) PCR [39]
B. microti USA‑native 0/3 PCR [54]
Babesia sp. Spain‑introduced 0/2 PCR [43]
B. vulpes 0/2
Hepatozoon spp. Hepatozoon sp. USA‑native 4/4 (100%) PCR [44]
H. canis Spain‑introduced 5/194 (2.57%) PCR [45]
Hepatozoon sp. USA‑native 3/15 (20%) PCR [39]
H. canis Spain‑introduced 0/2 PCR [43]
H. felis 0/2
H. martis 0/2
Borrelia spp. B. burgdorferi USA‑native 1/21 (4.8%) IFAT [46]
B. burgdorferi USA‑native 75/370 (20%) ELISA [47]
B. burgdorferi USA‑native 23/87 (26%) I FAT [48]
B. burgdorferi USA‑native 9/200 (4.5%) I FAT [49]
Borrelia sp.USA‑native IFAT 69/156 (44.23%) IFAT/PCR [50]
PCR 0/169
B. afzelii Japan‑introduced 1/752 (0.1%) IIA [55]
B. garinii 1/752 (0.1%)
B. lonestari USA‑native 1/19 (5.3%) IFAT [51]
B. burgdorferi USA‑native 0/30 I FAT [52]
B. turicatae USA‑native 2/25 (8%) Immunobloting [53]
B. burgdorferi USA‑native 1/39 (2.6%) PCR [54]
B. miyamotoi 0/39
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Table 1 (continued)
TBPs Species/genospecies Locality Prevalence Diagnostic test References
Rickettsia spp. R. rickettsi USA‑native 17/94 (18.1%) CF [56]
R. rickettsi USA‑native 35/129 (27.1%) IFAT [57]
R. montana 8/129 (6.2%)
R. bellii 369‑C strain 9/129 (6.9%)
R. rickettsi USA‑native 55/120 (45.8%) micro‑IF [58]
R. montana 1/120 (0.8%)
R. bellii 369‑C strain 2/120 (1.7%)
R. rickettsi USA‑native 3/14 (21.4%) MAT [59]
R. helvetica Japan‑introduced 11/699 (1.6%) PCR [62]
R. felis 1/699 (0.1%)
R. heliongjiangensis/R. japonica 1/699 (0.1%)
R. typhi USA‑native 0/9 IFAT [60]
R. japonica Japan‑introduced 14/752 (1.9%) IIA [55]
R. tsutsugamushi 39/752 (5.2%)
R. parkeri USA‑native 14/19 (73.7%) I FAT [51]
R. amblyommi Japan‑introduced 3/194 (1.5%) PCR [63]
Rickettsia sp. Hj126 3/194 (1.5%)
R. helvetica 1/194 (0.5%)
R. rickettsi USA‑native 3/30 (10%) I FAT [52]
Rickettsia sp. USA‑native 0/1 IFAT [61]
Rickettsia sp. USA‑native 3/39 (7.7%) PCR [54]
Bartonella spp. B. rochalimae USA‑native 11/42 (26%) PCR [65]
Bartonella sp.Japan‑introduced 0/977 PCR [69]
B. henselae USA‑native 12/37 (32.4%) PCR [66]
B. koehlerae 1/37 (2.7%)
B. clarridgeiae 0/37
B. rochalimae USA‑native 11/186 (5.9%) PCR [67]
B. berkhoffii 3/186 (1.6%)
Bartonella sp. USA‑native 0/39 PCR [54]
B.taylorii-like Canada‑native 1/1 (100%) PCR [68]
Anaplasma spp. A. phagocytophilum USA‑native IFAT 51/57 (89.5%) IFAT/PCR [70]
PCR 14/57 (24.6%)
A. phagocytophilum USA‑native IFAT 1/60 (1.7%) IFAT/PCR [71]
PCR 0/60
A. phagocytophilum Japan‑introduced IFAT 1/187 (0.5%) IFAT/PCR [73]
PCR 0/9
A. phagocytophilum USA‑native IFAT 1/156 (0.64%) IFAT/PCR [50]
PCR 0/169
A.phagocytophilum Japan‑introduced 0/699 PCR [72]
A. bovis 36/699 (5.15%)
Anaplasma sp.Austria‑introduced 0/4 PCR [28]
Anaplasma sp.Czech Republic‑introduced 0/15 PCR [6]
A. phagocytophilum Poland‑introduced 1/78 (1.3%) PCR [74]
Germany‑introduced 0/40
A. phagocytophilum USA‑native 15/39 (38.5%) PCR [54]
A. marginale 0/39
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Myśliwyetal. Parasites & Vectors (2022) 15:126
Rickettsia spp.
Studies related to Rickettsia species have been conducted
only in the native habitat of raccoon dogs, namely Japan
and South Korea. Neagari et al. [85] screened samples
from 30 raccoon dogs using serological tests with the aim
to detect R. japonica and R. tsutsugamushi antibodies;
however, none of the examined carnivores were infected
with these bacterial species. Other research carried out
in South Korea identified seropositive raccoon dogs, with
spotted fever group rickettsia (R. japonica) and typhus
group rickettsia (R. typhi) antibodies detected in 30.5%
and 41.6% of animals, respectively [86]. ese results are
Table 1 (continued)
TBPs Species/genospecies Locality Prevalence Diagnostic test References
Ehrlichia spp. E. chaffeensis USA‑native IFAT 9/43 (21%) IFAT [75]
E. chaffeensis USA‑native IFAT 83/411 (20%) IFAT/PCR [76]
PCR 0/20
E. canis USA‑native IFAT 13/60 (21.7%) IFAT/ PCR [71]
PCR 1/60 (1.7%)
E. chaffeensis IFAT 23/60 (38.3%)
PCR 0/60
E. ewingii PCR 0/60
E. canis Japan‑introduced IFAT 1/187 (0.5%) IFAT/PCR [73]
PCR 0/9
E. chaffeensis IFAT 3/187 (1.6%)
PCR 0/9
E. chaffeensis USA‑native IFAT 49/156 (31.41%) IFAT/PCR [50]
PCR 0/169
E. canis IFAT 18/156 (11.53%)
PCR 0/169
E. ewingii 0/169 PCR
E. chaffeensis USA‑native 8/19 (42.1%) IFAT [51]
E. chaffeensis Japan‑introduced 0/699 PCR [72]
E. canis 0/699
E. canis Austria‑introduced 0/4 PCR [28]
Ehrlichia sp.Czech Republic‑introduced 0/15 PCR [6]
E. canis Spain‑introduced 5/194 (2.57%) PCR [45]
E. canis USA‑native 0/39 PCR [54]
E. ewingii 0/39
E. chaffeensis 0/39
Candidatus Neoehrlichia sp. Candidatus Neoehrlichia lotoris USA‑native 32/60 (53.3%) PCR [71]
Candidatus Neoehrlichia lotoris USA‑native 131/197 (67%) PCR [78]
Candidatus Neoehrlichia sp. Czech Republic‑introduced 0/15 PCR [6]
Candidatus Neoehrlichia sp. Poland‑introduced 0//78 PCR [74]
Germany‑introduced 0/40
Prevalence and diagnostic tests are included for each reference
CF, Complement-xing antibodies; ELISA, enzyme-linked immunosorbent assay; IFAT, indirect uorescent antibody test, IIA, indirect immunoperoxidase assay; MAT,
microaglutination antibody test;PCR, polymerase chain reaction
a B. microti-like name was used for all sequences belonging to B. microti group and reported by authors as B. cf. microti
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Myśliwyetal. Parasites & Vectors (2022) 15:126
of great importance as the YH strain antigen (R. japon-
ica) used in the test on raccoon dogs is the same strain
used in the detection of seropositive humans in South
Korea. is study was the first time in South Korea that
wild animals were used as rickettsial infection indicators
[86]. Molecular studies undertaken by Han etal. [81] did
not show the presence of rickettsia species in any of 15
blood samples from raccoon dogs in South Korea.
Bartonella spp.
Research on this Gram-negativebacterium has been per-
formed only in Japan and South Korea. Early studies on
Bartonella in Japan confirmed DNA infection in 11 out
of 171 raccoon dogs; however, this pathogen was not
isolated from carnivores. e amplicons obtained were
most closely related to those of B. rochalimae which is an
emerging zoonotic pathogen in Europe, South America
and the USA [69, 87]. Molecular surveys of 619 Japa-
nese raccoon dogs (Nycetereutes procyonides viverrinus)
revealed the presence of B. rochalimae DNA in the blood
samples examined. However, this species has never been
detected in any other carnivore co-inhabiting the area
with the raccoon dogs, which suggests that raccoon dogs
specifically may be able to harbor this bacterium species
in their blood. Nevertheless, more research is needed to
confirm this hypothesis [88]. In another study, B. hense-
lae DNA was detected in blood and spleen samples of
raccoon dogs in South Korea [22].
Anaplasma spp.
Only two studies have been conducted in Asia on Ana-
plasma spp., both in South Korea. Han et al. [81] con-
firmed the first infection of A. bovis in Korean raccoon
dogs and suggested that they may act as a natural reser-
voir of this pathogen. However, only 15 samples of rac-
coon dogs were tested in this study, and only one sample
was PCR-positive for A. bovis. In a larger study which
was carried out subsequent to that Han etal. [81], Kang
etal. [22] examined 193 splenic tissue and blood samples
of Korean raccoon dogs; screening by PCR showed the
presence of A. bovis in 2.1% of the samples tested and,
for the first time, the presence of A. phagocytophilum in
1% of samples. Studies on this bacterium have also been
conducted in Europe. Anaplasma phagocytophilum has
been confirmed in raccoon dogs from Germany [89] and
Poland [90]. e study in Poland was the first in Europe
that involved a large number of raccoon dogs. Testing of
68 spleen samples showed that 24 samples (35.3%) were
positive for A. phagocytophilum. Other studies carried
out in Poland did not show the presence of Anaplasma
species [74] and neither did surveys carried out in the
Czech Republic [6] and Austria [28].
Ehrlichia spp. andCandidatus Neoehrlichia
To date, only one study has been conducted to detect
Ehrlichia spp. in the Korean native habitat of raccoon
dogs, and none of 15 blood samples examined was posi-
tive for this pathogen [82]. However, only a small num-
ber of carnivores were examined. Studies performed on
raccoon dogs in Austria [28] and Czech Republic [6] also
did not show the presence of Ehrlichia or Candidatus
Neoehrlichia spp. DNA. Research undertaken by Hilde-
brand etal. [74] revealed for the first time the presence
of Candidatus Neoehrlichia spp. (FU98) in raccoon dogs
from Poland and established the raccoon dog as a new
host for this pathogen. A detailed summary of currently
available data on TPBs in free-ranging raccon dogs is
provided in Table2.
Conclusions
A summary of the data originating from research car-
ried out mostly in the last two decades allows us to
conclude that the raccoon and raccoon dog are indeed
species with the potential to be competent reservoirs
of numerous TBPs. However, many epidemiological
aspects are still poorly understood, and more research
is required. It is exceptionally noteworthy that very few
studies on the incidence of TBPs in these carnivores
have been conducted in introduced areas. Both ani-
mals are alien species that have been introduced into
Europe, yet little or even no knowledge on the specific
TBPs they may harbor is available. erefore, many
opportunities for further research still exist. Future
studies should prioritize the testing of larger popula-
tions of introduced raccoons and raccoon dogs for the
presence of TBPs in areas where those animals have not
yet been sampled (or for which data are insufficient).
Results could then be compared with those obtained
from their native habitats. Moreover, the sympatric
occurrence of invasive and native carnivores facilitate
the inter-species transmission of pathogens and may
also play a relevant role in the circulation of pathogens
transmitted by ticks. Evaluation of possible cross-spe-
cies transmissions, vector establishment and an insight
into possible zoonotic implications appear to be essen-
tial for a better understanding of the epidemiology of
TBDs and to assess the potential risk originating from
these two invasive species.
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Myśliwyetal. Parasites & Vectors (2022) 15:126
Abbreviations
TBDs: Tick‑borne diseases; TBPs: Tick‑borne pathogens.
Authors’ contributions
JH conceived the paper. IM analyzed the data. IM and APH and wrote the
draft of the manuscript. APM and JH reviewed and edited the manuscript. All
authors read and approved the final version of the manuscript.
Funding
Not applicable.
Availability of data and materials
All data analyzed during this study is included in this published article.
Declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
Received: 28 October 2021 Accepted: 18 March 2022
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