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Background The bacteria of the genus Bartonella are obligate parasites of vertebrates. Their distribution range covers almost the entire world from America, Europe, Asia to Africa and Australia. Some species of Bartonella are pathogenic for humans. Their main vectors are blood-sucking arthropods such as fleas, ticks and blood-feeding flies. One such dipteran able to transfer vector-borne pathogens is the deer ked (Lipoptena cervi) of the family Hippoboscidae. This species acts as a transmitter of Bartonella spp. in cervid hosts in Europe. Methods In the present study, 217 specimens of deer ked (Lipoptena cervi) were collected from 26 red deer (Cervus elaphus) hunted in January 2014. A short fragment (333 bp) of the rpoB gene was used as a marker to identify Bartonella spp. in deer ked tissue by PCR test. A longer fragment (850 bp) of the rpoB gene was amplified from 21 of the positive samples, sequenced and used for phylogenetic analysis. Results The overall prevalence of Lipoptena cervi infection with Bartonella spp. was 75.12% (163/217); 86.67% (104/120) of females and 60.82% (59/97) of males collected from red deer hunted in the Strzałowo Forest District in Poland (53°45′57.03″N, 21°25′17.79″E) were infected. The nucleotide sequences from 14 isolates (Bartonella sp. 1) showed close similarity to Bartonella schoenbuchensis isolated from moose blood from Sweden (GenBank: KB915628) and human blood from France (GenBank: HG977196); Bartonella sp. 2 (5 isolates) and Bartonella sp. 3 (one isolate) were similar to Bartonella sp. from Japanese sika deer (GenBank: AB703149), and Bartonella sp. 4 (one isolate) was almost identical to Bartonella sp. isolated from Japanese sika deer from Japan (GenBank: AB703146). Conclusions To the best of our knowledge, this is the first report to confirm the presence of Bartonella spp. in deer keds (Lipoptena cervi) in Poland by molecular methods. Bartonella sp. 1 isolates were most closely related to B. schoenbuchensis isolated from moose from Sweden and human blood from France. The rest of our isolates (Bartonella spp. 2–4) were similar to Bartonella spp. isolated from Japanese sika deer from Japan. Electronic supplementary material The online version of this article (10.1186/s13071-017-2413-0) contains supplementary material, which is available to authorized users.
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R E S E A R C H Open Access
Molecular detection of Bartonella spp. in
deer ked (Lipoptena cervi) in Poland
Tomasz Szewczyk
, Joanna Werszko, Żaneta Steiner-Bogdaszewska, Witold Jeżewski, Zdzisław Laskowski
and Grzegorz Karbowiak
Background: The bacteria of the genus Bartonella are obligate parasites of vertebrates. Their distribution range
covers almost the entire world from America, Europe, Asia to Africa and Australia. Some species of Bartonella are
pathogenic for humans. Their main vectors are blood-sucking arthropods such as fleas, ticks and blood-feeding flies.
One such dipteran able to transfer vector-borne pathogens is the deer ked (Lipoptena cervi) of the family
Hippoboscidae. This species acts as a transmitter of Bartonella spp. in cervid hosts in Europe.
Methods: In the present study, 217 specimens of deer ked (Lipoptena cervi) were collected from 26 red deer
(Cervus elaphus) hunted in January 2014. A short fragment (333 bp) of the rpoB gene was used as a marker to
identify Bartonella spp. in deer ked tissue by PCR test. A longer fragment (850 bp) of the rpoB gene was amplified
from 21 of the positive samples, sequenced and used for phylogenetic analysis.
Results: The overall prevalence of Lipoptena cervi infection with Bartonella spp. was 75.12% (163/217); 86.67% (104/
120) of females and 60.82% (59/97) of males collected from red deer hunted in the Strzałowo Forest District in
Poland (53°4557.03N, 21°2517.79E) were infected. The nucleotide sequences from 14 isolates (Bartonella sp. 1)
showed close similarity to Bartonella schoenbuchensis isolated from moose blood from Sweden (GenBank: KB915628)
and human blood from France (GenBank: HG977196); Bartonella sp. 2 (5 isolates) and Bartonella sp. 3 (one isolate) were
similar to Bartonella sp. from Japanese sika deer (GenBank: AB703149), and Bartonella sp. 4 (one isolate) was almost
identical to Bartonella sp. isolated from Japanese sika deer from Japan (GenBank: AB703146).
Conclusions: To the best of our knowledge, this is the first report to confirm the presence of Bartonella spp. in deer keds
(Lipoptena cervi) in Poland by molecular methods. Bartonella sp. 1 isolates were most closely related to B. schoenbuchensis
isolated from moose from Sweden and human blood from France. The rest of our isolates (Bartonella spp. 24) were
similar to Bartonella spp. isolated from Japanese sika deer from Japan.
Keywords: Bartonella spp., Bartonella schoenbuchensis,Lipoptena cervi,Cervus elaphus
The genus Bartonella comprises small, Gram-negative
bacteria which act as obligate intracellular parasites of
vertebrates. About 30 species, as well as three subspe-
cies, have been described [1]. The zoonotic reservoir for
some Bartonella species (B. schoenbuchensis,B.bacili-
formis and B.quintana), is composed of wild mammals,
which usually only possess asymptomatic bacteraemia.
The prevalence of bacteremia in wild animals is often
very high, ranging from 50 to 95% in selected rodent
and ruminant populations [2, 3] and strongly depends
on the season [3]. As the reservoir hosts include a wide
range of wild mammals, including typically ruminants,
rodents and carnivores, the infections are easily spread
and have been noted all over the world [2]. A good ex-
ample is that of ruminant infections: Bartonella infec-
tion has been recorded in cattle in three different
countries (Thailand, Guatemala and Georgia) and in buf-
falo (Bubalus bubalis) from Thailand [4]. The prevalence
of Bartonella infection in these regions varies between
10 and 90%. Similar investigations in Japan found no in-
fection in cattle, but recorded a prevalence of Bartonella
* Correspondence:
Witold Stefański Institute of Parasitology, Polish Academy of Sciences, Twarda
51/55, 00-818 Warsaw, Poland
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Szewczyk et al. Parasites & Vectors (2017) 10:487
DOI 10.1186/s13071-017-2413-0
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sp., 67.5% in Honshu sika deer (Cervus nippon centralis)
and 50% in Yezo sika deer (Cervus nippon yesoensis) [5].
Many Bartonella species are considered as human
pathogens and causative agents of zoonotic diseases: B.
bacilliformis, the agent of Carrions disease and Verruga
peruna is the chronic delayed stage of infection; B.
quintana, the agent of trench fever and bacillary angio-
matosis; B. henselae, the agent of cat scratch disease and
of bacillary angiomatosis; B. clarridgeiae,B. elizabethae,
B.vinsonii subsp. arupensis,B.vinsonii subsp. berkhoffii,
B. alsatica,B. koehlerae and B. washoensis all cause
endocarditis [68]. The symptoms of human bartonello-
sis vary with regard to the bacterial species and general
condition of the patient; however, Bartonella infection
most often manifests as various cardiovascular, neuro-
logical and rheumatologic conditions [8, 9].
Bartonellosis has been observed in humans throughout
Europe, Asia and North America. One of the most im-
portant species is Bartonella schoenbuchensis, which is
found in cattle, wild animals (such as the cervids) and
humans [1012]. It has been identified in wild living roe
deer (Capreolus capreolus) in Germany [10], in cattle in
France [11] and in humans; B. schoenbuchensis was first
detected in France [12].
Bartonella are transmitted by blood-sucking arthro-
pods, such as lice, flies, fleas and ticks, many of which are
emerging pathogens of humans and animals [2, 1315].
Dehio et al. [16] identified B. schoenbuchensis in Lipoptena
cervi collected from red deer and roe deer. Halos et al.
[14] reported the presence of Bartonella spp. in hippobos-
cide flies, and suggested that flies can be a vector for path-
ogens. Other authors [14, 17] have found Bartonella spp.
in wingless adult deer keds.
Lipoptena cervi are blood-sucking parasites which
belong to a highly specialized family of louse flies
(Diptera: Hippoboscidae) [18, 19]. This species has a
Palaearctic distribution and occurs in Europe, Asia
and North America; it is known to be present in
many countries, including Sweden, Norway, Japan, the
USA and Finland [20, 21]. In America, it is regarded
as an invasive species, believed to have been
transported with deer from Europe in the 1800s. This
species was identified in the USA for the first time
during the Second World War [18]. In Europe, the
most common blood-sucking ectoparasites of
mammals belonging to this family are louse fly (Hip-
pobosca equina), parasitizing cows and horses, deer
keds (Lipoptena cervi and Lipoptena fortisetosa), para-
sitizing cervids, and sheep ked (Melophagus ovinus),
which ectoparasites of sheep [22, 23]. Lipoptena forti-
setosa in Europe could be introduced with Japanese
sika deer (Cervus nippon). This cervids were intro-
duced to England in 1860, and their number and
range have since increased [24]. From England, the
Japanese sika deer were late introduced to Poland,
where two species of Lipoptena have been identified:
L. cervi and L. fortisetosa [25, 26].
Although the dominant hosts for two species of Lipop-
tena (L. cervi and L.fortisetosa) are cervids (Alces alces,
Cervus elaphus,Cervus elaphus maral,Cervus nippon,
Dama dama,Capreolus capreolus and Rangifer tarandus),
the insects can attack a wide range of animals, including
bovids (Ovis aries musimon,Bison bonasus,cattle,Capra
aegagrus hircus and Ovis aries), carnivores (domestic dogs,
Vulpes vulpes and Meles meles) and suids (Sus scrofa)
[27]. The most important hosts of Lipoptena cervi in
Europe are red deer (Cervus elaphus), roe deer (Capreolus
capreolus), moose (Alces alces) and sika deer (Cervus
nippon), while Japanese sika deer (Cervus nippon) are the
predominate host in Japan, and white-tailed deer (Odocoi-
leus virginianus), moose (Alces alces) and cattle (Bos
taurus) in North America [21, 28, 29].
Generally, Lipoptena cervi is found swarming in large
numbers on the host. Deer keds most frequently bite
animal hosts; they can land on humans, but rarely bite
in this case. Nevertheless, some authors have reported
ked bites on humans [30, 31].
The life-cycle of Lipoptena cervi begins with free-
ranging, winged adult deer keds that search for a
suitable host (cervids). The winged deer keds usually
suck blood from the host and mate; however, after
landing on a host, they can crawl into the fur, shed
their wings and become permanently associated with
the oviduct and are then deposited in the cervid fur
as a white prepupa, which immediately starts to pupate.
The fully developed pupa drops to the ground and re-
mains there until August-September, when a new gener-
ation of winged adult deer keds can appear [29, 32, 33].
The female can produce to 2025 larvae per year. Lipop-
tena cervi can overwinter on the host, and most deer keds
can live to one year [34].
The winged adult Lipoptena cervi are attracted to large
moving dark-colored objects when actively searching for
a host [35]. Lipoptena cervi only fly for short distances
and frequently attack accidental hosts such as humans
or dogs [32].
Lipoptena cervi is a potential vector for other zoonotic
pathogens, such as Anaplasma,Borrelia and Rickettsia
species [36]. Korhonen et al. [37] showed for the first time
transstadial transmission of Bartonella spp. in all develop-
ment stages of deer ked (pupa, unfed adult winged deer
ked). These data show vector competence for transmis-
sion of Bartonella spp. by Lipoptena cervi. In America,
Bartonella sp. has been reported in Lipoptena cervi from
white-tailed deer in Massachusetts [28], and in Lipoptena
mazamae from white-tailed deer (Odocoileus virginianus)
in Georgia and South Carolina (USA) [21]. Additionaly, it
Szewczyk et al. Parasites & Vectors (2017) 10:487 Page 2 of 7
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has also been suggested that wingless adults of L. maza-
mae, could be transmitted mechanically from female
white-tailed deer to their offsprings [38]. Bartonella sp.
has also been found in ticks (Ixodes ricinus) parasitizing
roe deer in Poland [39].
The main goal of the study was detection of Bartonella
spp. DNA in Lipoptena cervi by PCR test and verifica-
tion of prevalence of this infection in adult wingless
males and females. Molecular characterization of speci-
mens of Bartonella spp. was done by analysis of partial
(850 bp) rpoB gene sequences.
Sample collection
Living deer keds (Lipoptena cervi) were collected from 26
red deer (Cervus elaphus) hunted in January 2014 in the
Strzałowo Forest District (53°4557.03N, 21°2517.79E).
After collection, all insects were preserved in 70% ethanol
for further morphological and molecular processing. Identi-
fication of deer ked (L. cervi) species and sex were con-
ducted using appropriate identification key [34] and
molecular methods to confirm vector species.
PCR and sequence analyses
In the laboratory, the flies were removed from 70% alcohol
and air-dried. The DNA was isolated from whole insect
body using the AX Tissue Mini kit (A&A Biotechnology,
Gdynia, Poland) according to the manufacturers protocol.
For PCR test the primers rpoR and rpoF were used.
These primers amplify a 333 bp fragment of the rpoB
gene of Bartonella spp. PCR reactions were conducted
according to Paziewska et al. [40]. 21 of 163 positive
samples were used to obtain a longer (850 bp) fragment
of the rpoB gene with second set of primers (1400F and
2300R) [41] (Table 1).
PCR reactions were conducted in a 50 μl reaction mixture
containing 2 μl of DNA template, 0.5 U (0.1 μl) of RUN Taq
polymerase (A&A Biotechnology, Gdynia, Poland), 1 μlof
dNTPs (10 mM), 0.5 μl of each primer (20 mM), and 5 μlof
10× Taq DNA polymerase buffer (pH 8.6, 25 mM MgCl
In the negative control, nuclease-free water was added to
the PCR mix instead of the tested DNA.
DNA amplification (1400F/2300R) was performed
using the DNA Engine PTC-200 Thermal Cycler
(BioRad, Hercules, USA) using the following program:
initial denaturation was performed at 94 °C for 5 min,
followed by 35 cycles of denaturation at 95 °C for 10 s,
annealing at 60 °C for 10 s and extension at 72 °C for
60 s. The final extension was performed at 72 °C for
7 min and then kept at 10 °C in a thermocycler.
The PCR products were visualized on a 1.0% agarose
gel stained with ethidium bromide. Visualization was
performed using ChemiDoc, MP Lab software (Imagine,
BioRad, Hercules, USA). The resulting product was
compared using the Nova 100 bp DNA Ladder Novazym
(Poznań, Poland). The PCR amplicons were purified
using a QIAEX II Gel Extraction Kit (Qiagen, Hilden,
Germany), sequenced in both directions by Genomed
(Poland) and contiguous sequences assembled using
ContigExpress, Vector NTI Advance 11.0 (Invitrogen
Life Technologies, New York, USA). The derived se-
quences were submitted to the GenBank database under
the accession numbers MF580655MF580675.
To confirm the morphological species determination of
Lipoptena cervi, DNA from four specimens (positive in
Bartonella spp. test and used in Bartonella isolate ana-
lysis), L700F and L1213R primers were used to amplify
and sequence 412 bp fragments of 16S rDNA (Table 1).
In order to perform PCR amplification, the following
mixture reaction was used: 4 μl of DNA extract was
added to 46 μl of reaction mixture consisting of 0.1 μlof
Allegro Taq Polymerase DNA (5 U/μl) (Poznań, Poland),
0.5 μl dNTPs (10 mM), 1 μl of each primer (20 mM),
5μl of 10× Taq DNA polymerase buffer (pH 8.6, 25 mM
), and 38.4 μl of deionized water.
DNA amplification (L700F/L1213R) was performed
using the DNA Engine PTC-200 Thermal Cycler
(BioRad, Hercules, USA) using the following program:an
initial denaturation was performed at 92 °C for 3 min,
followed by 35 cycles of denaturation at 95 °C for 10 s,
annealing at 60 °C for 10 s and extension at 72 °C for
30 s. The final extension was performed at 72 °C for
5 min and then kept at 12 °C in a thermocycler.
Phylogenetic analyses
We used Bayesian inference (BI) analysis with MrBayes
version 3.2 [42]. Analysis of partial rpoB gene sequence
data was based on an alignment of 804 bp (268 amino
acids) using the GTR + I + G model. The GTR models
were chosen on the basis of jModelTest version 2.1.4
[43, 44] using the Akaike information criterion.
In total, 217 deer keds were collected from 26 red deer
(Cervus elaphus). All insects were identified as Lipop-
tena cervi using morphological features [34]. The preva-
lence of Bartonella spp. infection was 75.12% (163/217)
by PCR test. In the tested group of L. cervi, a greater
Table 1 List of primers sequences used in this study
Primer Sequence (5-3) Reference
rpoR CGCATTATGGTCGTATTTGTCC Paziewska et al. [40]
1400F CGCATTGGCTTACTTCGTATG Renesto et al. [41]
2300R GTAGACTGATTAGAACGCTG Renesto et al. [41]
Szewczyk et al. Parasites & Vectors (2017) 10:487 Page 3 of 7
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proportion of females (86.67%) was found to be positive
for Bartonella spp. than males (60.82%).
PCR, sequence and molecular analyses
Fourteen sequences (Bartonella sp. 1: MF580662
MF580675) obtained in this study share over 99% similarity
with B. schoenbuchensis isolated from moose blood from
Sweden (GenBank: KB915628) and from human blood
from France (GenBank: HG977196). Five sequences Barto-
nella sp. 2 (MF580657MF580661) showed 94.6% similar-
ity with Bartonella sp. 3, and 94.4% with Bartonella sp.
from Japanese sika deer from Japan (AB703149). Bartonella
sp. 3 (MF580656) showed 99.7% similarity with another
samples isolated from Japanese sika deer from Wakayama
Prefecture Japan (AB703149). Bartonella sp. 4 (MF580655)
was 99,7% similar with Bartonella sp. isolated from
Japanese sika deer (Cervus nippon centralis)fromNaraPre-
fecture Japan (AB703146). These results are summarized in
Table 2 and Additional file 1: Table S1.
Four 16S rDNA sequences of deer ked were obtained,
which were identical with Lipoptena cervi collected in the
Czech Republic (AF322437). The sequences derived dur-
ing this study were submitted to the GenBank database
under the accession numbers MF541726MF541729.
Our findings indicate the presence of Bartonella species
in deer keds (Lipoptena cervi) obtained from red deer
(Cervus elaphus). Dehio et al. [16] noted that L. cervi
appears to be a natural reservoir supporting the trans-
mission of Bartonella schoenbuchensis. The largest group
of isolates (Bartonella sp. 1) showed closed similarity
with Bartonella schoenbuchensis. Our data indicate a
high prevalence of Bartonella spp. A prevalence of
75.12% was recorded in the whole tested group, a result
similar to global data; however, higher values were
observed in Finland (90%) and France (94%) [14, 37].
Table 2 Bartonella spp. used in the phylogenetic analysis
Isolate/sequence ID Species Host Source Country of isolation
MF580662MF580675 Bartonella sp. 1 Lipoptena cervi whole body Poland
MF580657MF580661 Bartonella sp. 2 Lipoptena cervi whole body Poland
MF580656 Bartonella sp. 3 Lipoptena cervi whole body Poland
MF580655 Bartonella sp. 4 Lipoptena cervi whole body Poland
DQ356077 Bartonella bovis bovine blood Italy
EF432062 B. bovis cow valve (heart) France
KR733195 B. bovis cattle blood Malaysia
KR733194 B. bovis cattle blood Malaysia
KF218224 B. bovis water buffalo blood Thailand
KF218220 B. bovis cattle blood Thailand
KF218218 B. bovis cattle blood Guatemala
KF218217 B. bovis cattle blood France
HM167505 Bartonella capreoli moose blood USA
AB703143 B. capreoli Japanese sika deer blood Japan
AB703142 B. capreoli Japanese sika deer blood Japan
AB703149 Bartonella sp. Japanese sika deer blood Japan
AB703146 Bartonella sp. Japanese sika deer blood Japan
AB703145 Bartonella sp. Japanese sika deer blood Japan
KB915628 Bartonella schoenbuchensis moose blood Sweden
KM215709 Bartonella chomelii cattle blood Spain
KM215710 Bartonella chomelii cattle blood Spain
JN646664 Bartonella chomelii cattle blood New Caledonia
KJ909808 Bartonella bovis cattle blood Israel
AB703148 Bartonella sp. Japanese sika deer blood Japan
AB703144 Bartonella sp. Japanese sika deer blood Japan
HG977196 Bartonella schoenbuchensis human blood France
CP019789 Bartonella schoenbuchensis European roe deer blood Germany
Szewczyk et al. Parasites & Vectors (2017) 10:487 Page 4 of 7
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To the best of our knowledge, the present paper is the
first report in Poland to identify differences in the preva-
lence of Bartonella spp. infection in male and female
deer keds. Females were more frequently infected than
males; 86.67% of wingless females were infected by
Bartonella, similar to a study from Hungary (76.0%),
while only 60.82% of wingless males were infected, also
similar to a result in Hungary (58%) [45].
lence is not clear; however, it might be associated
with the multiple bites needed for larvae production
(2025 larvae per year) [34]. De Bruin et al. [45]
suggested that Bartonella species are able to colonize
or survive more efficiently as females than males, but
the molecular mechanism for this remains unknown.
The same authors [45] suggested that Bartonella spp.
infection in female deer keds might lead to more
female offspring than uninfected females, possibly
resulting in the observed asymmetry in the female:-
male ratio of infected individuals.
By transmitting pathogens, Lipoptena cervi can be po-
tentially dangerous for animals and humans. A study
Fig. 1 Phylogenetic tree of Bartonella spp., constructed by Bayesian inference (BI) analysis using MrBayes version 3.2. For BI codon analysis
(nucmodel = codon), the GTR + I + G model was chosen based on jModelTest version 2.1.4 [43, 44] using Akaike Information Criterion. Analysis
was run for 8,000,000 generations, with 2,000,000 generations discarded as burn-in. Hosts, country and GenBank accession numbers of origin are
shown. Nodal support is indicated as Bayesian posterior probabilities. Sequence from Brucella melitensis (AY562179) was used as outgroup.
Sequences generated in this study are shown in bold
Szewczyk et al. Parasites & Vectors (2017) 10:487 Page 5 of 7
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
conducted in Finland found that L. cervi can transmit
some pathogens by biting, and this is associated with
hair-loss epizootics in moose [17]. Since the 1970s, in
Finland an increasing number of cases of recurrent, and
occasionally long-lasting, dermatitis associated with deer
keds bites has been observed [46].
Fourteen of the sequences (Bartonella sp.1,seeTable2.)
isolated from deer keds demonstrated 99.2% homology with
aBartonella schoenbuchensis sample isolated from moose
in Sweden (KB915628). Bartonella schoenbuchensis could
be found in vectors, such as L. cervi or L. mazamae,orin
definitive hosts like cattle, wild ruminants and humans [10,
11, 16]. It is difficult to see how the relationship between B.
schoenbuchensis and deer ectoparasites may relate to simi-
lar cases in humans. Lipoptena cervi has fed on humans
under experimental conditions and in the natural environ-
ment [18, 47]. As humans may be infected with B. schoen-
buchensis during occasional biting by L. cervi, hunters,
forestry workers and cross-country runners, among others,
are at increased risk of infection [16]. Although L. cervi has
not yet been definitively demonstrated to transmit B.
schoenbuchensis through bites, it is possible that hunters
are at risk to infection of Bartonella schoenbuchensis or
Anaplasma phagocytophilum following exposure to deer
blood [48].
In Massachusetts, a Bartonella sp. similar to B. schoen-
buchensis has been found in Lipoptena mazamae [21],
which suggests that Lipoptena species can extend the
range of B. schoenbuchensis. Our phylogenetic analysis of
the partial rpoB gene sequences found that our samples
were in the same clade as other B. schoenbuchensis isolates
from moose (KB915628) and human (HG977196). Barto-
nella schoenbuchensis (strain closely related to B. schoen-
buchensis strain R186.6%, gltA gene) was previously
reported from roe deer (C. capreolus) in Poland [49].
Bartonella sp. 2 (5 isolates) and Bartonella sp. 3
(MF580656) demonstrated high similarity to sequences
obtained from Japanese sika deer from Japan
(AB703149, 94.6% and 99.7% similarity, respectively.
These Bartonella isolates are related with the B. bovis
clade in our phylogenetic analysis (Fig. 1).
Bartonella sp. 4 (MF580655) is very similar (99.7%) to
Bartonella sp. isolates collected from Japanese sika deer
(AB703146, see Fig. 1) and in our phylogenetic analyses
these isolates are associated with other Bartonella sp.
isolates from Japanese sika deer and formed a distinct
clade with Bartonella spp. isolated from Japanese sika
deer. Probably japaneseBartonella isolates were intro-
ducted to Poland. This observation suggests that the
strain of Bartonella sp. bacteria identified in the present
study is derived from Japanese sika deer introduced to
Europe by vectors to environment, indicating that this
Asian strains could be spread by L. cervi to European
red deer (Cervus elaphus).
Some Japanese Bartonella sp. samples, isolated from
different prefectures, comprise a group distinct from
other samples of Bartonella on GenBank; however, fur-
ther testing is required utilizing other genes, including
gltA and ftsZ, to confirm whether they could be regarded
as a distinct species.
Our data confirm that Bartonella spp. can be transmitted
by deer ked in central Europe, and the prevalence of this
pathogen is very high. In this area, Lipoptena cervi are
infected by various species of the genus Bartonella.
Additional files
Additional file 1: Table S1. Pairwise comparison of partial (804 bp)
mitochondrial gene rpoB DNA and amino acid sequences variability
among species/sequences of Bartonella used in phylogenetical analysis.
Above diagonal: number of variable sites in the 268 amino acid gene
rpoB sequences. Below diagonal: number of variable sites in the
nucleotides gene rpoB sequences. The percentage of variable sites for
each gene fragment between 2 species/sequences is given in
parenthesis. Each species isolates/sequence information are provided in
Table 2. (DOCX 23 kb)
The authors would like to express their gratitude to Marek Bogdaszewski,
Head of the Research Station in Kosewo Górne (W. Stefański Institute of
Parasitology), for enabling us to collect the samples from red deer.
No funding was received.
Availability of data and materials
The data supporting the conclusions of this article are included within the
article and its additional file. The sequences were submitted to the GenBank
database under the accession numbers MF580655MF580675 (Uncultured
Bartonella sp.) and MF541726MF541729 (Lipoptena cervi).
TS planned and organized the study. JW and ŻSB collected samples. TS and
JW extracted DNA. ZL performed PCR, sequencing and analyzed sequence
data. TS, WJ and ZL drafted the manuscript, and wrote the final version
together with GK. All authors read and approved the final manuscript.
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in
published maps and institutional affiliations.
Received: 21 April 2017 Accepted: 29 September 2017
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... A similarly high percentage (33.3%) of L. fortisetosa infected by this bacteria collected from a different animal host in the area of eastern Poland, was shown by Bartosik et al. [25]. Szewczyk et al. [26] showed that the overall prevalence of infection with Bartonella spp. was 75.12% among L. cervi collected from red deer. Gałęcki et al. [11] detected the DNA of these pathogens in 63.2% of L. fortisetosa. ...
... Haplotype H1 of Bartonella sp. (host L. fortisetosa), representing lineage D, grouped with haplotypes described in Poland by Szewczyk et al. [26] (GenBank Acc. No. MF580657), and in Japan by Sato et al. [18] (GenBank Acc. ...
... Nos. AB703149 and LC485121, respectively) and in Poland [26] (GenBank Acc. No. MF580656). ...
Full-text available
Deer keds are hematophagous ectoparasites (Diptera: Hippoboscidae) that mainly parasitize Cervidae. These flies are particularly important for animal health due to the occurrence of numerous pathogenic microorganisms. They may also attack humans and their bites may cause allergenic symptoms. The aim of the study was to identify the molecular characteristics of Borrelia burgdorferi sensu lato and Bartonella spp. pathogens detected in Lipoptena spp. sampled both from the hosts and from the environment. For identification of Bartonella spp and B. burgdorferi s. l., the primers specific to the rpoB and flaB gene fragments were used, respectively. The overall prevalence of B. burgdorferi s.l. DNA in Lipoptena cervi was 14.04%, including 14.8% infection in the tested group of winged specimens. The overall prevalence of Bartonella spp. was 57.02%. The presence of these bacteria was detected in 53.5% of specimens of L. cervi and 75.7% of L. fortisetosa. The phylogenetic analysis showed five new haplotypes of the rpoB gene of Bartonella sp. isolated from L. cervi/Lipoptena fortisetosa. We also identified one new haplotype of B. afzelii and three haplotypes of B. burgdorferi isolated from winged specimens of L. cervi. This is the first study to detect the genetic material of B. burgdorferi s.l. in L. cervi in Poland and the first report on the identification of these bacteria in host-seeking specimens in the environment.
... These species pose a threat to wildlife, livestock and pets (Halos et al., 2004;Hermosilla et al., 2006;Kynkäänniemi et al., 2014;Metelitsa and Veselkin, 1989), and create a pathway for zoonotic pathogens to jump between reservoir hosts and accidental hosts (Malmsten et al., 2019). The biological material (DNA) of many pathogens has been identified in deer keds (Bartosik & Maślanko, 2021;Gałęcki et al., 2021b;Hornok et al., 2011;Lee et al., 2016;Regier et al., 2018;Szewczyk et al., 2017;Werszko et al., 2020). Furthermore, these blood-feeding ectoparasites can also bite humans during the recreational use of forests Maślanko and Bartosik, 2020). ...
... (Hornok et al., 2011), Bartonella spp. (Duodu et al., 2013;Szewczyk et al., 2017) and Rickettia spp. (Hornok et al., 2011) have also been detected in this species. ...
Full-text available
The louse flies of the genus Lipoptena spp. (Diptera: Hippoboscidae) are obligate blood-feeding species and potential vectors of several pathogens. These ectoparasites are known for their potential harm to wild animals. This review summarized the recent research on Lipoptena spp.’s role as potential vectors of pathogens and the impact of climate change on their distribution. The review focused on the biological characteristics, medical and veterinary significance, rapid geographic expansion, and challenges in controlling Lipoptena spp. Finally, we provided some considerations for future research on the Lipoptena spp.
... Lipoptena cervi has also been widely reported to be infected with Bartonella spp. (Peña-Espinoza et al., 2023;Regier et al., 2018;Szewczyk et al., 2017). Bird-specialized louse flies have also been reported to transmit epidemiologically important pathogens, but they seem highly understudied in this context. ...
... Frontiers in Veterinary Science 09 has previously been found in L. cervi and L. fortisetosa collected from red deer in Poland (62,64). These findings suggest novel Bartonella stains from wild ruminants in Japan may spread to other countries following Lipoptena vector introduction into these new areas. ...
Full-text available
Lipoptena insects are important ectoparasites of cervids and may affect humans that are incidentally bitten. The presence of zoonotic pathogen DNA, such as Anaplasma , and Bartonella , raises the importance of Lipoptena insects in veterinary and human medicine. Eld’s deer ( Rucervus eldii thamin ), an endangered wild ruminant in Thailand, are bred and raised in the open zoo. The semi-wild zoo environment suggests ectoparasite infestation and potential risk for mechanical transmission of pathogens to visitors, zoo workers, or other animals. However, epidemiology knowledge of pathogens related to endangered wild ruminants in Thailand is limited. This study aims to determine the prevalence and diversity of Anaplasma and Bartonella in the L. fortisetosa collected from captive Eld’s deer in Chon Buri, Thailand. Of the 91 Lipoptena DNA samples obtained, 42 (46.15%) and 25 (27.47%) were positive for Anaplasma and Bartonella by molecular detection, respectively. Further, 42 sequences of Anaplasma (4 nucleotide sequence types) showed 100% identity to those detected in other ruminants and blood-sucking ectoparasites. Twenty-five sequences of Bartonella (8 nucleotide sequence types) showed 97.35–99.11% identity to the novel Bartonella species from sika deer and keds in Japan. Phylogenetic trees revealed Anaplasma sequences were grouped with the clusters of A. bovis and other ruminant-related Anaplasma , while Bartonella sequences were clustered with the novel Bartonella species lineages C, D, and E, which originated from Japan. Interestingly, a new independent lineage of novel Bartonella species was found in obtained specimens. We report the first molecular detection of Anaplasma and Bartonella on L. fortisetosa , which could represent infectious status of captive Eld’s deer in the zoo. Wild animals act as reservoirs for many pathogens, thus preventive measures in surrounding areas should be considered to prevent pathogen infection among animals or potential zoonotic infection among humans.
... were described in L. cervi (75.12%) and L. fortisetosa (63.2%) in Poland27,7 . Similarly higher values were observed in Finland (90%) and France (90%)8,32 . ...
Full-text available
Lipoptena cervi and Lipoptena fortisetosa are hematophagous ectoparasites from the Hippoboscidae family that mainly parasitizes Cervidae. These species may also attack humans and its bites may cause allergenic symptoms. The aim of the study was to determine the role of Lipoptena species as a potential vector and/or reservoir of Borrelia burgdorferi sensu lato and Bartonella spp. pathogens in forested areas of north-eastern Poland. The presence of B. burgdorferi s.l was shown in 16.6% of L. cervi . Bartonella spp. was detected in 53.5% of L. cervi and in 75.7% of L. fortisetosa , respectively. The conducted study confirmed the presence of Bartonella spp. in L. cervi and L. fortisetosa . The first evidence of Borrelia bugdorferii s.l. in winged specimens of L. cervi was shown. The obtained data indicates that deer keds can harbor these pathogens, but further investigations are required to confirm that Lipoptena could be a biological vector of these pathogens.
... Moreover, they can play an important role as carriers of pathogens, mainly Anaplasma spp., Bartonella spp., Borrelia spp., Coxiella spp., Theileria spp., and Trypanosoma spp. [11][12][13][14][15][16][17]. Recently, the Asian species L. fortisetosa has colonized most European countries, including Italy, where it is competing with L. cervi for territories and host microniches [18]. ...
Full-text available
Lipoptena cervi (Linnaeus), Lipoptena fortisetosa Maa, Hippobosca equina Linnaeus, and Pseudolynchia canariensis (Macquart) are hematophagous ectoparasites that infest different animal species and occasionally bite humans. Hosts are located by a complex process involving different kinds of stimuli perceived mainly by specific sensory structures on the antennae, which are the essential olfactory organs. General antennal morphology, together with distribution and ultrastructure of sensilla, have been studied in detail with scanning and transmission electron microscopy approaches. Observations have revealed some common features among the four studied hippoboscids: (a) typical concealment of the flagellum inside the other two segments; (b) characteristic trabecular surface of the flagellum; (c) peculiar external microtrichia; (d) presence on the flagellum of basiconic sensilla and grooved peg coeloconic sensilla; (e) unarticulated arista. The ultrastructure of L. fortisetosa revealed that microtrichia and the flagellar reticulated cuticle are not innervated. Different roles have been hypothesized for the described antennal structures. Microtrichia and the reticulated cuticle could convey volatile compounds towards the flagellar sensory area. Peculiar sensory neurons characterize the unarticulated arista which could be able to detect temperature variations. Coeloconic sensilla could be involved in thermoreception, hygroreception, and carbon dioxide reception at long distances, while the poorly porous basiconic sensilla could play a role in the host odour perception at medium–short distances.
... [21][22][23][24][25][26], Bartonella spp. [23,[27][28][29][30][31][32][33][34], Borrelia spp. [24,35], Ehrlichia spp. ...
Full-text available
Background White-tailed deer ( Odocoileus virginianus ) host numerous ectoparasitic species in the eastern USA, most notably various species of ticks and two species of deer keds. Several pathogens transmitted by ticks to humans and other animal hosts have also been found in deer keds. Little is known about the acquisition and potential for transmission of these pathogens by deer keds; however, tick-deer ked co-feeding transmission is one possible scenario. On-host localization of ticks and deer keds on white-tailed deer was evaluated across several geographical regions of the eastern US to define tick-deer ked spatial relationships on host deer, which may impact the vector-borne disease ecology of these ectoparasites. Methods Ticks and deer keds were collected from hunter-harvested white-tailed deer from six states in the eastern US. Each deer was divided into three body sections, and each section was checked for 4 person-minutes. Differences in ectoparasite counts across body sections and/or states were evaluated using a Bayesian generalized mixed model. Results A total of 168 white-tailed deer were inspected for ticks and deer keds across the study sites. Ticks ( n = 1636) were collected from all surveyed states, with Ixodes scapularis ( n = 1427) being the predominant species. Counts of I. scapularis from the head and front sections were greater than from the rear section. Neotropical deer keds ( Lipoptena mazamae ) from Alabama and Tennessee ( n = 247) were more often found on the rear body section. European deer keds from Pennsylvania (all Lipoptena cervi , n = 314) were found on all body sections of deer. Conclusions The distributions of ticks and deer keds on white-tailed deer were significantly different from each other, providing the first evidence of possible on-host niche partitioning of ticks and two geographically distinct deer ked species ( L. cervi in the northeast and L. mazamae in the southeast). These differences in spatial distributions may have implications for acquisition and/or transmission of vector-borne pathogens and therefore warrant further study over a wider geographic range and longer time frame. Graphical Abstract
Full-text available
Background: Livestock are key sources of livelihood among pastoral communities. Livestock productivity is chiefly constrained by pests and diseases. Due to inadequate disease surveillance in northern Kenya, little is known about pathogens circulating within livestock and the role of livestock-associated biting keds (genus Hippobosca ) in disease transmission. We aimed to identify the prevalence of selected hemopathogens in livestock and their associated blood-feeding keds. Methods: We randomly collected 389 blood samples from goats (245), sheep (108), and donkeys (36), as well as 235 keds from both goats and sheep (116), donkeys (11), and dogs (108) in Laisamis, Marsabit County, northern Kenya. We screened all samples for selected hemopathogens by high-resolution melting (HRM) analysis and sequencing of PCR products amplified using primers specific to the genera: Anaplasma, Trypanosoma, Clostridium, Ehrlichia, Brucella, Theileria, and Babesia. Results: In goats, we detected Anaplasma ovis (84.5%), a novel Anaplasma sp. (11.8%), Trypanosoma vivax (7.3%), Ehrlichia canis (66.1%), and Theileria ovis (0.8%). We also detected A. ovis (93.5%), E. canis (22.2%), and T. ovis (38.9%) in sheep. In donkeys, we detected ‘ Candidatus Anaplasma camelii’ (11.1%), T. vivax (22.2%), E. canis (25%), and Theileria equi (13.9%). In addition, keds carried the following pathogens; goat/sheep keds - T. vivax (29.3%) , Trypanosoma evansi (0.86%), Trypanosoma godfreyi (0.86%), and E. canis (51.7%); donkey keds - T. vivax (18.2%) and E. canis (63.6%); and dog keds - T. vivax (15.7%), T. evansi (0.9%), Trypanosoma simiae (0.9%) , E. canis (76%), Clostridium perfringens (46.3%), Bartonella schoenbuchensis (76%), and Brucella abortus (5.6%). Conclusions: We found that livestock and their associated ectoparasitic biting keds carry a number of infectious hemopathogens, including the zoonotic B. abortus . Dog keds harbored the most pathogens, suggesting dogs, which closely interact with livestock and humans, as key reservoirs of diseases in Laisamis. These findings can guide policy makers in disease control.
The deer ked Lipoptena mazamae (Diptera: Hippoboscidae) (Róndani), is a blood‐feeding obligate ectoparasite of several species of deer and brocket. However, at present little information is available about its role as a vector of hemoparasites. Nonetheless, it is considered a competent vector for the transmission of Bartonella species. The aim of this study was performing the morphological and molecular identification of ked flies and to carry out the detection of Bartonella. We collected specimens from Chiná, Campeche, Mexico associated with white‐tailed deer. Using polymerase chain reaction (PCR), of COI, gltA and rpoB genes, we were able to obtain the first barcode for L. mazamae from Mexico and identified a new species of Bartonella which was found with a prevalence of 73%. The data obtained in this study confirmed the presence of L. mazamae associated with white‐tailed deer and its possible role as vector of Candidatus Bartonella odocoilei n. sp. in Mexico and we considered that it may also be present in white‐tailed deer populations in the U.S.A. Additional investigations into Bartonella species associated with deer ked could provide further insight into their pathogenicity and its role as a zoonotic agent. The deer ked Lipoptena mazamae was identified using the COI gene for the first time for Mexico. Bartonella sp. was detected in deer ked in Campeche; using rpoB and gltA genes, we detected a new linage temporarily named as Candidatus Bartonella odocoilei. The role of Lipoptena mazamae in the transmission of Candidatus Bartonella odocoilei, in Campeche is very probable, however, additional entomological surveys are necessary.
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Bats are important reservoirs for many zoonotic pathogens. However, no surveys of bacterial pathogens in bats have been performed in the Caucasus region. To understand the occurrence and distribution of bacterial infections in these mammals, 218 bats belonging to eight species collected from four regions of Georgia were examined for Bartonella, Brucella, Leptospira, and Yersinia using molecular approaches. Bartonella DNA was detected in 77 (35%) bats from all eight species and was distributed in all four regions. The prevalence ranged 6–50% per bat species. The Bartonella DNA represented 25 unique genetic variants that clustered into 21 lineages. Brucella DNA was detected in two Miniopterus schreibersii bats and in two Myotis blythii bats, all of which were from Imereti (west-central region). Leptospira DNA was detected in 25 (13%) bats that included four M. schreibersii bats and 21 M. blythii bats collected from two regions. The Leptospira sequences represented five genetic variants with one of them being closely related to the zoonotic pathogen L. interrogans (98.6% genetic identity). No Yersinia DNA was detected in the bats. Mixed infections were observed in several cases. One M. blythii bat and one M. schreibersii bat were co-infected with Bartonella, Brucella, and Leptospira; one M. blythii bat and one M. schreibersii bat were co-infected with Bartonella and Brucella; 15 M. blythii bats and three M. schreibersii bats were co-infected with Bartonella and Leptospira. Our results suggest that bats in Georgia are exposed to multiple bacterial infections. Further studies are needed to evaluate pathogenicity of these agents to bats and their zoonotic potential.
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Background: The deer ked (Lipoptena cervi) is an ectoparasite on cervids that has invaded large parts of Norway, Sweden and Finland during recent decades. During their host-seeking flight activity, the adult deer keds constitute a considerable nuisance to people and limit human outdoor recreation. The bites of the deer ked can cause long-lasting dermatitis in humans. Determining the pattern of flight activity during autumn is hence important. Methods: Data on flight phenology was gathered by walking along transects in the forest in two counties of Norway during 2009-2013, counting the number of host-seeking keds. We analysed how the flight activity of deer keds varied depending on date and prevailing weather during autumn. Results: The best model of flight activity included both date and temperature, both as nonlinear terms. Host-seeking deer keds were observed from early August to mid-November with a marked peak in late September. Number of host-seeking keds declined with temperatures falling below the mean, but did not increase much at above mean temperatures. The pattern of flight phenology was similar across the two counties and five years. Conclusions: Parasitic arthropods may be strongly affected by prevailing weather during off-host periods. Our study shows an estimated positive effect of temperature on deer ked flight activity mainly for below mean temperatures in late autumn, while the effect of temperature on flight activity in early autumn was weak. The pattern of host-seeking flight activity during late, rather than early autumn, is hence more likely to change with ongoing climate change, with a predicted increase in duration of the host-seeking period.
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Certain Bartonella species are known to cause afebrile bacteremia in humans and other mammals, including B. quintana, the agent of trench fever, and B. henselae, the agent of cat scratch disease. Reports have indicated that animal-associated Bartonella species may cause paucisymptomatic bacteremia and endocarditis in humans. We identified potentially zoonotic strains from 6 Bartonella species in samples from patients who had chronic, subjective symptoms and who reported tick bites. Three strains were B. henselae and 3 were from other animal-associated Bartonella spp. (B. doshiae, B. schoenbuchensis, and B. tribocorum). Genomic analysis of the isolated strains revealed differences from previously sequenced Bartonella strains. Our investigation identifed 3 novel Bartonella spp. strains with human pathogenic potential and showed that Bartonella spp. may be the cause of undifferentiated chronic illness in humans who have been bitten by ticks.
Borrelia burgdorferi and Anaplasma phagocytophilum are obligate intracellular parasites that maintain their life cycles in enzoonotic vector-host cycles with Ixodes scapularis as a vector. In addition to ticks, the hosts are commonly infested with insects from the Hippoboscidae family. This study confirms the presence of B. burgdorferi and A. phagocytophilum in deer keds (Lipoptena cervi) removed from white-tailed deer using PCR. Detection of these pathogens in deer ked represents a potential novel susceptibility of wildlife and also suggests the risk of transmission of these pathogens to humans and animals alike through the bite of an infected ectoparasite. This study represents the first instance in the U.S. of detection of tick-borne pathogens in a member of the Hippoboscid family.
The aim of this study was to identify the species of ked infesting dogs in the cities of central Poland. A total of 510 dogs were observed between June and September 2015. The presence of keds was noted in 182 (35.7%) animals. Keds were more prevalent in female (38.0%) than in male (33.2%) dogs, and were more frequently found in animals younger than 1 year (46.2%) and in long-haired dogs (36.6%). The body areas most heavily colonized by keds were the groin (35.4%) and neck (21.4%). A total of 904 keds were isolated from dogs, including Hippobosca equina (Diptera: Hippoboscidae) (17.2%), Lipoptena cervi (Diptera: Hippoboscidae) (32.0%), and two species not previously encountered in Poland: Hippobosca longipennis (45.0%) and Lipoptena fortisetosa (5.9%). Hippoboscidae may act as vectors of pathogens and any shifts in their geographic range may lead to the spread of new diseases affecting animals.
Ticks are vectors for many bacterial, protozoan and viral pathogens and are potential vectors for Bartonella species. Hunters and foresters, therefore, may be regarded as high-risk groups for Bartonella infections. The aims of this study were (i) to identify Bartonella species in questing Ixodes ricinus ticks collected in all provinces of Austria, and (ii) to determine the prevalence of antibodies to Bartonella species in hunters and blood donors in eastern Austria. A total of 515 larval, nymphal and adult I. ricinus, collected throughout Austria in 2005, were selected from the tick library at the Institute for Hygiene and Applied Immunology of the Medical University of Vienna and screened in a specific real-time PCR that targeted a region of the ssrA gene of Bartonella species. The overall Bartonella infection rate was 2.1% (11/515) and the highest rate, 7.5% (4/53), was found in ticks from Vienna. This finding was confirmed by screening a further 60 I. ricinus collected from Vienna in 2013: of these, 6.7% (4/60) were positive for Bartonella spp. The rate of infection was always higher in adult ticks. Sequence analysis in the Bartonella-positive ticks identified several species, including B. henselae, B. doshiae and B. grahamii. To our knowledge this is the first time that these species have been identified in I. ricinus in Austria. Prevalence of IgG antibodies against B. henselae and B. quintana was determined in serum samples from hunters (100) and blood donors (100): in hunters 23% were positive for B. quintana and in 2 samples (2%), antibodies to both B. quintana and B. henselae were detected; in blood donors 22% were positive for B. quintana, 1% for B. henselae and 5% for both. These results indicate that exposure to ticks does not constitutes a relevant risk for Bartonella infection.
Improved epidemiological surveillance and use of new diagnostic techniques has enabled the recent discovery or provided improved information on existing infections of numerous zoonoses of bacterial origin. The main factors causing emergence or re-emergence include changes to the environment, intensive production of food products and growth of international transport of these products, human demography and behaviour, as well as bacterial adaptation to a new environment. An emergence or re-emergence of bacterial zoonoses originating from food (salmonellosis, Escherichia coli infections, etc.). resulting from pets (salmonellosis, plague, Q fever), associated with immunodepression (Rhodococcus equi infection, Bartonella henselae infection, etc.) or due to vectoral transmission (Lyme disease, ehrlichiosis, etc.) has been observed (4 figures, 1 table, 1 box, 43 references).