Campylobacter in wintering great tits Parus major in Poland

Abstract

Domestic and wild mammals, domestic birds and particularly wild birds are considered to be reservoirs of many species of Enterobacteriaceae, and also important human enteric pathogens, e.g., the bacteria of the genus Campylobacter that occur in their digestive tracts. These species may be vectors of antimicrobial resistance dissemination in the environment, because they may have contact with an environment contaminated with antibiotics. Bird feeders have been suggested as potential dispersal centres between wild wintering birds whose feeding is supported by humans. Therefore, we checked for the presence of Campylobacter bacteria among great tits Parus major, the most common bird species on bird feeders in Poland. Samples (n = 787 cloacal swabs) were collected in urban and rural areas of Poland. Bacterial species were identified using multiplex PCR, and 23 (2.9%) positive tests for Campylobacter spp. were found; in ten samples, C. jejuni was detected. The odds ratio of Campylobacter infection in rural birds was over 2.5 times higher than urban birds. Ten samples with C. jejuni were tested for antibiotic resistance, and all were sensitive to azithromycin, erythromycin and gentamycin, while six isolates were resistant to tetracycline, and five were resistant to ciprofloxacin. Four Campylobacter isolates were resistant to both these antibiotics.

Full text

RESEARCH ARTICLE
Campylobacter in wintering great tits Parus major in Poland
Piotr Tryjanowski
1
&Jacek J. Nowakowski
2
&Piotr Indykiewicz
3
&Małgorzata Andrzejewska
4
&Dorota Śpica
4
&
RafałSandecki
5
&Cezary Mitrus
6
&Artur Goławski
7
&Beata Dulisz
2
&Joanna Dziarska
1
&Tomasz Janiszewski
8
&
Piotr Minias
8
&Stanisław Świtek
1
&Marcin Tobolka
1
&Radosław Włodarczyk
8
&Bernadeta Szczepańska
4
&
Jacek J. Klawe
4
Received: 2 March 2019 / Accepted: 22 December 2019
#Springer-Verlag GmbH Germany, part of Springer Nature 2019
Abstract
Domestic and wild mammals, domestic birds and particularly wild birds are considered to be reservoirs of many species of
Enterobacteriaceae, and also important human enteric pathogens, e.g., the bacteria of the genus Campylobacter that occur in
their digestive tracts. These species may be vectors of antimicrobial resistance dissemination in the environment, because they
may have contact with an environment contaminated with antibiotics. Bird feeders have been suggested as potential dispersal
centres between wild wintering birds whose feeding is supported by humans. Therefore, we checked for the presence of
Campylobacter bacteria among great tits Parus major, the most common bird species on bird feeders in Poland. Samples (n=
787 cloacal swabs) were collected in urban and rural areas of Poland. Bacterial species were identified using multiplex PCR, and
23 (2.9%) positive tests for Campylobacter spp. were found; in ten samples, C. jejuni was detected. The odds ratio of
Campylobacter infection in rural birds was over 2.5 times higher than urban birds. Ten samples with C. jejuni were tested for
antibiotic resistance, and all were sensitive to azithromycin, erythromycin and gentamycin, while six isolates were resistant to
tetracycline, and five were resistant to ciprofloxacin. Four Campylobacter isolates were resistant to both these antibiotics.
Keywords Antibiotic resistance .Birds .Campylobacteriosis .Farmland .Microbes .Urbanization
Introduction
Campylobacteriosis is a disease caused by bacteria of the ge-
nus Campylobacter that occurs in the digestive tract of farm
and domestic animals (poultry, cattle, pigs, dogs, cats) and
wild animals (both birds and mammals) (Wieczorek and
Osek 2013; Waldenström and Griekspoor 2014;Haldetal.
2015). Campylobacter includes several dozen species and
subspecies, and the bacteria transmitted to humans can cause
gastrointestinal infections. In humans, diarrhoea is most often
Responsible editor: Robert Duran
Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s11356-019-07502-y) contains supplementary
material, which is available to authorized users.
*Piotr Tryjanowski
piotr.tryjanowski@gmail.com
1
Institute of Zoology, PoznańUniversity of Life Sciences, Wojska
Polskiego 71C, 60–625 Poznań, Poland
2
Department of Ecology and Environmental Protection, University of
Warmia and Mazury in Olsztyn, Plac Łódzki 3, 10–
727 Olsztyn, Poland
3
Department of Biology and Animal Environment, University of
Technology and Life Sciences, Ks. A. Kordeckiego 20, 85–
225 Bydgoszcz, Poland
4
Department of Hygiene, Epidemiology and Ergonomics, Nicolaus
Copernicus University, M. Curie Skłodowskiej 9, 85–
094 Bydgoszcz, Poland
5
J. Kusocińskiego 19/71, Inowrocław, Poland
6
Department of Vertebrate Ecology and Paleontology, Institute of
Biology, Wrocław University of Environmental and Life Sciences,
Chełmońskiego 38c, 51-631 Wrocław, Poland
7
Department of Zoology, Siedlce University of Natural Sciences and
Humanities, Prusa 12, 08–110 Siedlce, Poland
8
Department of Teacher Training and Biodiversity Studies, University
of Łódź, Banacha 1/3, 90–237 Łódź,Poland
Environmental Science and Pollution Research
https://doi.org/10.1007/s11356-019-07502-y

caused by Campylobacter jejuni (90–95% of all infections
caused by Campylobacter species and about 5% caused by
Campylobacter coli). Together with salmonellosis, it is one
of the most frequently reported diseases of the gastrointestinal
tract, a serious problem in many countries.
Reports of the European Food Safety Authority (EFSA)
and the European Centre for Disease Prevention and Control
(ECDC) show that campylobacteriosis was the most frequent-
ly confirmed zoonosis in the European Union (EU), whose
prevalence and the number of detected cases have been in-
creasing since 2008 (EFSA 2015,2017). Wild birds are con-
sidered reservoirs of human intestinal pathogens and vectors
for the propagation of antibiotic resistance in the environment.
Several studies have demonstrated the important role of mi-
gratory birds in the circulation and spread of enterogenic hu-
man pathogens, such as Campylobacter,Salmonella,
Escherichia coli-producing toxins and antimicrobial resistant
organisms (Reed et al. 2003; Abulreesh et al. 2007;Fotietal.
2011,2017; Magda et al. 2013), and so may aid in the spread
of antimicrobial-resistant organisms.
An important problem in the high invasiveness of
Campylobacter strains is the acquisition of antibiotic resis-
tance. Campylobacter has, like other Eubacteria,the
Restriction-Modification immune system, which acts as a de-
fence mechanism against the invasion of foreign genomes
(Visu and Nagaraja 2013). For example, resistance to cipro-
floxacin and tetracycline may be caused by a one-point muta-
tion that has pleiotropic effects. The other mutation, cfxB,
conferred pleiotropic resistance to ciprofloxacin, tetracycline
and chloramphenicol and appeared to be an allele of the mul-
tiple antibiotic resistance gene marA (Hooper et al. 1987). The
presence of drug resistance in a bacterium does not necessarily
result from direct contact between wild birds and poultry (for
which there is a high proportion of drug-resistant strains), but
such genes could have been taken from other bacteria, bacte-
riophages, or even from the environment. Several authors
have suggested that farm animals are a source of significant
quantities of antibiotics in the soil in agriculture landscapes,
with the consequent introduction of resistance genes and re-
sistant bacteria (Binh et al. 2009; Byrne-Bailey et al. 2009;
Gaze et al. 2011). Gillings and Stokes (2012), and Gillings
(2013) consider that antibiotics and resistance genes, as well
as new xenobiotic elements selected due to exposure to anti-
biotics, may be important pollutants of the environment. The
important sources of antibiotic transmissions into the agricul-
tural environment are wastes from veterinary use and live-
stock farming. Pollution from pharmaceuticals in surface
and groundwater is becoming recognized as an environmental
concern in manycountries leading to the area of study labelled
PIE –Pharmaceuticals in the Environment (Khetan and
Collins 2007). Several studies have demonstrated the wide
dissemination of antibiotic-resistant enterobacteria in popula-
tions of birds inhabiting areas of high densities of livestock
and humans (Camarda et al. 2006; Literak et al. 2010;
Elmberg et al. 2017). However, information on the presence
of potential pathogens in wild birds is still limited, and the
understanding of their role as vectors in pathogen transmission
is insufficient (Foti et al. 2011,2017;Haldetal.2015). In
many studies, it is pointed out that anthropogenic factors in
the urban environment may reduce immunity and affect the
function of resistance genes, which could promote infections.
On the other hand, the release of antibiotics into the environ-
ment in agricultural areas may favour the spread of antibiotic-
resistant pathogens (Hald et al. 2015; Wieczorek and Osek
2015). Based on data related to the level of antibiotic con-
sumption (Wojkowska-Mach et al. 2018) and occurrence of
antimicrobial agents in the biggest river (Vistula) and other
freshwaters in Poland (Gbylik-Sikorska et al. 2014;
Giebułtowicz et al. 2018;Szymańska et al. 2019), it can be
assumed that in Polish conditions, the transfer of antibiotics
from cultures and strains originating from livestock farms to
the soil together with the increasingly popular practice of ma-
nure spreading from intensive livestock farms is an important
infection vector, especially antibiotically resistant C. jejuni
strains. However, it is not clear how birds from different en-
vironments, for example, farmland and urban areas, differ in
their prevalence of Campylobacter.
Therefore, the main aim of the current study was to char-
acterize the frequencies of Campylobacter occurrence in the
great tit Parus major during winter. The great tit is a common
species widely distributed in Poland (Kuczyński and
Chylarecki 2012), also in urban and rural environments, and
moves into urban areas in winter, probably largely due to
improved feeding conditions provided by man (Van Balen
1973; Lehikoinen 1986;Orell1989), and is the most common
species using feeders (Tryjanowski et al. 2015). In the winter,
great tits and other species gather in groups near human set-
tlements and very often use bird feeders, which influence the
frequency of contacts between individuals (Tryjanowski et al.
2017) and, therefore, the spread of pathogens. Thus the fre-
quency of Campylobacter spp.occurrence in great tits in ur-
ban and rural environments was determined. The resistance to
antibiotics of isolated C. jejuni was tested, which may be
important for assessing the role of birds as reservoirs of path-
ogens and the possibility of their transmission.
Materials and methods
Study area
The research was carried out in five cities and eight near-
by villages located in central and north-eastern Poland
(Fig. 1). Each city site had at least one linked rural site
located within 30 km from the city centre. The study
involved two cities with a human population below
Environ Sci Pollut Res

100,000, one in the range 100–200,000 and two over
200,000 (Table 1).
Field methods
Birds were caught in ornithological mist nets in the vicinity of
bird feeders in winter. Before capture session, birds were
attracted by additional feed for a few days. Birds were caught
no earlier than 1 h after sunrise. Captures were conducted in
two periods, 1st catch, 10 December 2015 to 10 February
2016, and 2nd catch, 11 February to 20 March 2016, in order
to cover the beginning and the end of the winter period.
During capture, birds were marked with alphanumeric orni-
thological rings to avoid repeated sampling. Recaptured indi-
viduals were not sampled for Campylobacter occurrence a
second time. During ringing, birds were sexed, aged,
Table 1 Information on study sites
City/village Code Urban/rural Number of residents
(thous.)
Geographical coordinates Surrounding Distance to nearest livestock
(km)
NE
Inowrocław INO U 74.8 52.79 18.26 Residential, gardens 3.1
Siedlce SIĘU 76.7 52.17 22.27 Residential 2.1
ŁodźLOD U 722.0 51.77 19.46 City centre 3.0
PoznańPOZ U 552.4 52.41 16.93 Buildings, park 4.8
Olsztyn OL U 175.5 53.78 20.48 Agriculture, forests 7.0
Węgierskie WEG R 0.2 52.33 17.25 Agriculture 0.2
Grodztwo GRO R 0.6 52.67 18.35 Agriculture 0.3
Bartołty Wielkie WM R 0.2 53.79 20.83 Agriculture, forests 0.5
Topórek TOP R 0.2 52.19 22.31 Agriculture 0.5
Teodorów TEO R 0.3 52.13 22.20 Agriculture, forests 0.9
Golice GOL R 0.5 52.21 22.34 Agriculture 0.1
Nowa Gadka NOG R 0.2 51.68 19.43 Agriculture, Residential 3.0
Łask LAS R 18.1 51.59 19.13 Residential 3.2
Fig. 1 Study area, cities (U, urban) and villages (R, rural)
Environ Sci Pollut Res

measured (length of wing and tail) and weighed according to
the standard procedure used in the biometry of birds
(Svensson 1992).
After capture, a cloacal swab was collected using the
Transwab® ENT Amies Charcoal transported medium
(Medical Wire & Equipment, Corsham, England) and labelled
with an individual code. Transwab was kept at 1–4°Cuntil
arrival at the laboratory. All collected samples were taken to
the Microbiology Laboratory of the Department of Hygiene
and Epidemiology of Nicolaus Copernicus University in
Bydgoszcz within 12–18 h and analysed upon arrival.
Laboratory methods
Campylobacter isolation, detection and susceptibility testing
The material used in laboratory investigations were cloacal
swabs stored in Transwab® ENT Amies Charcoal transported
medium. According to the procedure described earlier by
French et al. (2009), cloacal swabs were put into 3 ml of
Bolton broth (Oxoid Limited, Basingstoke, UK) for the
preincubation step. Incubation conditions were as follows:
temperature 42 °C, time 48 h, microaerobic atmosphere
(Generbox microaer-BioMerieux, Marcy l’Etoile, France).
After preincubation, the suspension from Bolton broth was
spread on agar plates (modified Charcoal Cefoperazone
Desoxycholate Agar-Oxoid Limited, Basingstoke, UK).
After incubation under microaerobic atmosphere, bacterial
growth from CCDA plates was spread to a blood plate
(Columbia agar with 5% cattle blood-Oxoid Limited,
Basingstoke, UK). Columbia plates were incubated in the
same conditions as CCDA plates. Characteristic bacterial
growth was transferred to Microbanks (Pro-Lab Diagnostics,
UK) and stored at −80 °C for further examination.
For isolation of bacterial DNA, the classic boiling method,
described by De Lamballerie et al. (1992), was used. Bacterial
cultures were suspended in 100 μl of PBS (Oxoid Limited,
Basingstoke, UK), boiled with 45 μl of chelating resin
(Chelex 100-BioRad, Hercules, USA) and then centrifuged
at 13,000 x g for 10 min.
Molecular identification of Campylobacter species was
carried out using the multiplex PCR reaction with primers
and amplification conditions described by Yamazaki-
Matsune et al. (2007). This reaction simultaneously detects
Campylobacter coli,Campylobacter jejuni,Campylobacter
fetus,Campylobacter hyointestinalis subsp. hyointestinalis,
Campylobacter lari and Campylobacter upsaliensis –the
most common human and animal pathogens. The composition
of the PCR reaction mixture included 5 μl of PCR Buffer
(Thermo Fisher Scientific, Waltham, USA), 0.5 μlofdNTPs
(10 mm Thermo Fisher Scientific, Waltham, USA), 1 μlof
each primer (1 μM) and 1 U Dream Taq DNA polymerase
(Thermo Fisher Scientific, Waltham, USA). Primers for the
PCR reaction were synthesized by the Institute of
Biochemistry and Biophysics Polish Academy of Sciences
(Warsaw, Poland). Visualization of DNA paths was obtained
by adding the Midori Green DNA Stain (Nippon Genetics,
Duren, Germany) to 1% agar gel prior electrophoresis. The
size of the amplicon was compared with DNA size marker
100 bp (Thermo Fisher Scientific, Waltham, USA). The
PCR results were visualized using the IG/LE InGenius L doc-
umentation system (Syngene, Cambridge, UK). Within col-
lected samples out of 23 Campylobacter spp., ten were iden-
tified as C. jejuni. After identifying the species of
Campylobacter, strains were tested for antimicrobial suscep-
tibility using E-test (BioMerieux, Marcy l’Etoile, France) on
Mueller-Hinton agar with 5% defibrinated horse blood (Oxoid
Limited, Basingstoke, UK). Incubation of Mueller-Hinton
plates was made in accordance with the manufacturer’srec-
ommendations. Antimicrobials chosen for susceptibility tests
in this study were: erythromycin, azithromycin, tetracycline,
ciprofloxacin and gentamicin. Macrolides and
fluoroquinolones are considered to be the first choice drug
for the treatment of campylobacteriosis in humans.
Tetracyclines, gentamicin and azithromycin are alternative
drugs. In addition, tetracycline is used in veterinary medicine
in Poland. The reference to Campylobacter resistance analy-
ses was the breakpoints for Enterobacteriaceae family de-
scribed by Clinical and Laboratory Standards Institute (CLSI
2008), which were as follows for specific antimicrobials:
erythromycin 32 μg/mL, tetracycline 16 μg/mL, azithromycin
8μg/mL, ciprofloxacin 4 μg/mL and gentamicin 8 μg/mL.
C. jejuni ATCC 33560 and C. coli ATTC 33559 were used as
reference strains.
Statistical methods
Prediction of Campylobacter presence in birds depending on
the type of environment (urban or rural) was analysed by a
generalized linear model for the binomial distribution of de-
pendent data (0, absence; 1, presence), using logit function
and maximum likelihood estimation method.
The assessment of the risk of Campylobacter infection de-
pending on the type of population (rural vs. urban) was based
on the odds ratio (OR), commonly used in epidemiological
studies (Riffenburgh 2006).
Results
Of the 787 swabs analysed, 23 (2.9%) samples contained
Campylobacter, and, among these, 10 samples were positive
for the presence of C. jejuni (Appendix 1).
The probability of Campylobacter presence was higher in
rural than urban birds (GLM model, log-likelihood = 101.298,
chi-square = 4.87, p=0.027).
Environ Sci Pollut Res

Similar results were shown in the other analyses. The odds
ratio showed that the chances of Campylobacter colonization
in the group of rural birds were over 2.5 times higher than in
the group of urban birds (OR = 2.674; 95% C.I 1.077–6.508;
chi square = 4.84, df = 1, p= 0.028). Although the lower con-
fidence limit of the odds ratio estimate is close to 1 (indicating
the same probability of infection in both groups), there was a
significantly higher infection rate in the rural environment
compared to urban. The sensitivity of the analysis is quite
high, assessed as the probability of truly positive results (sen-
sitivity = 0.696).
All isolated Campylobacter jejuni were sensitive to
azithromycin, erythromycin and gentamicin, while six were
refractory to tetracycline, and five were refractory to cipro-
floxacin. Four of C. jejuni were resistant to both antibiotics,
i.e., ciprofloxacin and tetracycline.
Sampling sites at urban environment were significantly
further away from the nearest livestock farms than sites in a
rural environment (Mann-Whitney test, U = 4.5; Z = 2.196,
p= 0.028). Significant negative relationships were found be-
tween the distance of sampling sites (catching birds) from the
nearest livestock farms and the number of samples with pos-
itive tests of Campylobacter occurrence (Kendall rank corre-
lation coefficient: r
t
=−0.57, n= 13, p= 0.006) in a given
place.
Discussion
In the studied wintering great tits in Poland, the prevalence of
Campylobacter was relatively low (2.9%) in comparison to
other studies of birds. However, it is difficult to show any clear
pattern because the prevalence of Campylobacter ssp. varies
considerably between different geographical regions, habitats
of birds, different species and ecological birds groups. In dif-
ferent habitats and regions, the prevalence in wild birds varied
significantly. High prevalence of Campylobacter spp.in wild
birds (12.5–24.2%) was reported from New Zealand (French
et al. 2009), Iran (Abdollahpour et al. 2015), Japan (Shyaka
et al. 2015) and Chile (Fernandez et al. 1996), while very low
Campylobacter occurrence was found in studies of birds from
Northern England (1.4%) (Hughes et al. 2009)andtheUSA
(7.2%) (Keller et al. 2011). Data from Waldenström et al.
(2002) and Waldenström and Griekspoor (2014) show that
certain species or ecological groups appear to be colonized
more frequently than others. Especially high prevalence was
noted in Anatidae (27.1–54.5%), Charadridae (33.3–86.2%),
Scolopacidae (74.0%), Laridae (44.9%) and Columbidae
(10.3–100%) and among passerines in Corvidae (48.7–
100%), Sturnidae (35.1–41.2%) and Turdidae (12.6–37.9%).
Among different ecological groups, high prevalence was re-
ported among shoreline-foraging and aquatic invertebrate
feeders (33.3–76.8%, Waldenström et al. 2002), pheasants
(44%; Dipineto et al. 2008), wild urban birds (33%; Mohan
2015), raptors (33.1%, Gargiulo et al. 2018; 12.6%,
Waldenström et al. 2002), ground-foraging insectivores
(20.3%) and herbivorous (18.8%, Waldenström et al. 2002).
Trying to explain the difference between the prevalence of
Campylobacter spp. in great tits in our study (2.9%) and the
data presented by Mohan (2015) from New Zealand urban
environments (33% Campylobacter spp., 19%
Campylobacter jejuni), is probably related to local species
composition and ecological groups of birds. High prevalence
in wild urban birds in Mohan’s studies may result from col-
lection of samples from the faeces of water birds (ducks,
swans, geese) and starlings, which, as shown in the data
above, belong to high prevalence groups. Overall, prevalence
in water birds was at a high level, e.g., 67.4% in Chile
(Fernandez et al. 1996), also in Poland –88.4% (Krawiec
et al. 2017). Among Passerines, starlings belong to a group
with high prevalence, which may result from foraging in
meadows and fields in agriculture landscapes. Differences in
the prevalence of Campylobacter jejuni in different species
may also be due to the dynamics of bird colonization by
different strains. Research by Atterby et al. (2018)showed,
in experiments, that C. jejuni host-specific strains had differ-
ences in their ability to colonize mallards, more likely associ-
ated with host origin, rather than the author’s suggestion that
differences might be explained by observed host association
patterns in C. jejuni from wild birds.
It is also not surprising in our study that the most frequently
diagnosed Campylobacter species was C.jejuni, which is the
most common species recognized in wild birds, as well as in
poultry (Szczepańska et al. 2015;Haldetal.2015).
Campylobacter jejuni was frequently isolated between differ-
ent species of Campylobacter (69.5% up to 94.1% of
Campylobacter spp. isolates (Fernandez et al. 1996;Keller
et al. 2011; Shyaka et al. 2015; Szczepańska et al. 2015).
The higher prevalence in rural than in urban birds is probably
related to a higher prevalence of Campylobacter reservoirs in
the environment. Similarly, in human populations living in
rural areas, the risk of campylobacteriosis was 1.89-fold
higher than in urban areas (Lévesque et al. 2013). The main
source of Campylobacter infections was occupational expo-
sure to animals, and 64.5% of human C. jejuni isolates were
attributable to chicken. In our studies, the highest prevalence
in great tits was found in a rural area in Golice. In the vicinity
of this village (within a radius 2.0 km from where birds were
caught), five poultry farms occur. The high number of positive
samples from Golice determines the importance of differenti-
ating the degree of bird infection by the type of environment
(urban/rural). However, regardless of whether this sample re-
mains in the analysis or is removed, there is a strong negative
correlation between the distance between sampling sites
(catching birds) from the nearest animal farm and the number
of positive samples found (Kendall rank correlation
Environ Sci Pollut Res

coefficient: sample with data from Golice: r
t
=−0.57, n=13,
p= 0.006; sample without data from Golice: r
t
=−0.48, n=
12, p= 0.029). This suggests that the distance from the envi-
ronment that allows the frequency of contact with livestock is
important here, and this frequency is obviously higher in the
rural environment than urban. Hald et al. (2015)foundasig-
nificant correlation between the prevalence of C. jejuni in wild
birds and the proportion ofthe bacteria in manure on cattle and
poultry farms. The results of this study along with previous
research suggest that that wild birds feeding on fields fertilized
with liquid manure (e.g., groups mentioned above often in-
fected with Campylobacter) or synanthropic birds having con-
tact with livestock farms may constitute an important reservoir
of Campylobacter in the natural environment.
The most frequent phenotypic resistance in the isolated
Campylobacter jejuni strains was against tetracycline (6 out
of 10 isolates). The antibiotic tetracycline is frequently used in
veterinary medicine in Poland. The presence of highly resis-
tant strains to tetracycline was previously listed among
Campylobacter isolated from other animal sources, such as
poultry, cattle and pigs (Wieczorek and Osek 2013,2015).
However, there is much less information on estimates of the
prevalence of antibiotic resistance in wild birds. The C. jejuni
strains isolated from white stork Ciconia ciconia in Poland
described by Szczepańska et al. (2015) show resistance
against ciprofloxacin (52.4%) and tetracycline (19%).
Jurado-Tarifa et al. (2016) revealed a similar level of resis-
tance to tetracycline in C. jejuni isolated from wildfowl and
raptors to those observed in our study. These authors also
suggested that the increasing antimicrobial resistance among
environmental Campylobacter strains can have effects on hu-
man and animal epidemiology of campylobacteriosis.
Campylobacter resistance to fluoroquinolones, which are rec-
ommended for the treatment of campylobacteriosis in
humans, is a public health problem. Reported by EFSA
(2014), the emergence of fluoroquinolone resistance among
Campylobacter strains isolated from farm animals (poultry,
pigs and cattle) or directly from chicken meat is an important
issue for human health. In studies by Chuma et al. (2000),
23% of strains of C. jejuni isolated from sparrow faeces
showed quinolone resistance, and they emphasize the possi-
bility of acquiring quinolone-resistant C. jejuni strains due to
contact with domestic animals and their feed.
To conclude, Campylobacter prevalence in Polish great tits
was low, though it was detected more frequently in rural birds
near livestock farms. Although recognized as sedentary birds,
great tits very often migrate from forest and rural to urban
areas in winter, due to the higher temperature and easier access
to food and increase survival rate (Lehikoinen 1986; Orell
1989; Tryjanowski et al. 2015). Therefore, while they can be
considered as a potential epidemiological factor to humans,
especially to ornithologists catching birds and also probably to
people feeding birds, this impact is probably very low.
Acknowledgements Ł. Myczko for assistance during the field work, an
anonymous referee for very useful comments, and T.H. Sparks for
English language editing.
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