Eur J Wildl Res (2004) 50: 127–132
DOI 10.1007/s10344-004-0052-1
O R I GI N A L P A P E R
Ksenija Vlahović Æ Biserka Matica Æ Ingeborg Bata
Marina Pavlak Æ Željko Pavičić Æ Maja Popović
Srebrenka Nejedli Æ Alenka Dovč
Campylobacter, salmonella and chlamydia in free-living birds
of Croatia
Received: 25 April 2004 / Accepted: 20 July 2004 / Published online: 13 August 2004

Springer-Verlag 2004
Abstract Campylobacteriosis, salmonellosis and avian
chlamydiosis are zoonotic diseases in which birds have
been suggested to play an important role as reservoirs.
We have investigated the prevalence of Campylobacter
and Salmonella spp. and Chlamydophila sp. in 107 free-
living birds belonging to 25 species from 13 families
from Croatia in order to examine the natural infections
caused by these agents. Campylobacter jejuni-like
organisms were isolated from 2 of 107 free-living bird
species examined (1.9%). Salmonella was isolated from 8
fresh fecal specimens from free-living bird species
(7.4%). These isolates were identified as S. typhimurium
in 4 (3.7%), and S. enteriditis in 4 (3.7%) free-living
birds. These samples originated from feral pigeons
(Columba livia domesticus; n=14; 28.6%), rook (Corvus
frugilegus; n=13; 15.4%), buzzard (Buteo buteo; n=12;
16.7%), black-headed gull (Larus ridibundus; n=8;
12.5%) and tawny owl (Strix aluco; n=8; 12.5%). The
K. Vlahović (&) Æ M. Pavlak Æ M. Popović
Department of Biology, Faculty of Veterinary Medicine,
University of Zagreb, Heinzelova 55,
10 000 Zagreb, Croatia
E-mail: vlahovic@vef.hr
B. Matica
Zagreb Public Health Institute, Mirogojska cesta 16,
10 000 Zagreb, Croatia
I. Bata
Association for Wildlife and Environmental Protection (AWAP),
Siget 6, 10 000 Zagreb, Croatia
Ž. Pavičić
Department of Animal Hygiene, Environment and Ethology,
Faculty of Veterinary Medicine, University of Zagreb,
Heinzelova 55, 10 000 Zagreb, Croatia
S. Nejedli
Department of Anatomy, Histology and Embryology,
Faculty of Veterinary Medicine, University of Zagreb,
Heinzelova 55, 10 000 Zagreb, Croatia
A. Dovč
Institute for Health Care of Poultry,
University of Ljubljana, Cesna v Mesni log 47,
Ljubljana, Slovenia
presence of Chlamydophila sp. was not detected in the
free-living birds examined during this study. Epidemio-
logical aspects and possible significance of the examined
birds as a source of infections for domestic animals and
humans are discussed.
Keywords Campylobacter Æ Salmonella Æ
Chlamydophila Æ Free-living birds
Introduction
Free-living bird species are a significant component of
the human environment. They transmit over 40 diseases
to domestic animals and humans, including salmonel-
losis, tuberculosis, histoplasmosis, toxoplasmosis, chl-
amydiosis, cryptococcosis, encephalitis, Newcastle
disease, aspergillosis, blastomycosis, candidiasis, and
sarcosporidiosis (Weber 1979a, 1979b; Stickley and
Weeks 1985). The role of free-living birds in the trans-
mission of such diseases to domestic animals, produc-
tion poultry and especially to humans, has been well
documented by many authors (Kapperud and Rosef
1983; Al-Sallamis 1991; Cizek et al. 1994; Literak et al.
1995; Fernández et al. 1996; Adesiyun et al. 1998;
Chuma et al. 2000; Craven et al. 2000; Jeffrey et al. 2001;
Giammanco et al. 2002; Broman et al. 2004). Avian
influenza A viruses can be transmitted from free-living
birds to mammals and humans (OIE 2000b). Zoonoses
are generally transmitted from free-living birds to
humans directly by contact, arthropod vectors or food.
Public health threats result from the accumulation of
bird fecal droppings (Lenhart et al. 1997).
Numerous domestic and wild animal species,
including mammals and birds, have been identified as
natural reservoirs of Campylobacter (Rosef 1981;
Kapperud and Rosef 1983; Ito et al. 1988; Levre et al.
1989; Hubalek et al. 1995; Fernández et al. 1996;
Adesiyun et al. 1998; Jeffrey et al. 2001). Feral pigeons
showed frequent infection with C. jejuni (Kinjo et al.
128
1983) and seagulls were frequently infected with
C. jejuni, C. coli, or C. lari (Kaneuchi et al. 1987).
Salmonella typhimurium can cause serious disease in
humans, especially in the young, old or persons with
diseases that may compromise the immune system. The
main route of transmission is likely to be via fecal con-
tamination of food at feeding sites. Salmonella species
can survive severe conditions, and under suitable con-
ditions, multiply in the environment (Kapperud and
Rosef 1983; Brittingham and Temple 1988; Brittingham
et al. 1988; Keymer 1993; Cizek et al. 1994; Gerlach
1994b; Kirkwood and Macgregor 1998; Prescott et al.
1998; Tizard 2004).
Avian chlamydiosis (AC) is caused by the bacterium
Chlamydophila psittaci (Everett and Andersen 1997;
Everett et al. 1999). Chlamydiosis in birds is often
systemic and infections can be inapparent, severe,
acute or chronic with intermittent shedding. Stress will
commonly trigger onset of severe symptoms, resulting
in rapid deterioration and death (Andersen and Van-
rompay 2000; OIE 2000a). Young birds are more
susceptible than adults and the disease can spread
rapidly among colonial nesting birds (Burkhart and
Page 1971; Brand 1989; Grimes 1994). Chlamydiosis
might be transferred by translocation of birds of prey
and could also be spread during falconry bird flight
(Forbes 1997).
C. jejuni (8.7%), S. typhimurium (7.4%) and Myco-
bacterium avium intracellulare (0.26%) have been iso-
lated from diseased feral pigeons in Croatia (Gregurić
et al. 1991). The humoral immune responses to
Chlamydophila sp. in domestic and free-living bird spe-
cies in Croatia have been assayed (Vlahović et al. 1998;
Pavlak et al. 2000). Monitoring of free-living bird
diseases is of considerable importance, especially since
free-living birds are increasingly kept in centers for
rehabilitation purposes and reintroduction programs are
conducted. In this context, an investigation of diseases
of free-living birds is important.
The objective of the present study was to determine
the occurrence of Campylobacter sp., Salmonella sp. and
Chlamydophila sp. in free-living birds from Croatia in
order to monitor such diseases with zoonotic potential
for transmission to other animals and humans.
Materials and methods
Birds
A total of 107 free-living birds that originated from
Croatian territory were examined, including 14 feral
pigeons (Columba livia var. domestica), 8 black-headed
gulls (Larus ridibundus), 1 greater black-backed gull
(Larus marinus), 4 barn owls (Tyto alba), 2 long-
eared owls (Asio otus), 8 tawny owls (Strix aluco), 11
eagle owls (Bubo bubo), 4 little owls (Athene noctua), 1
ural owl (Strix uralensis), 3 bitterns (Botaurus stellaris),
1 gray heron (Ardea cinerea), 1 northern harrier (Circus
cyanneus), 12 buzzards (Buteo buteo), 1 white-tailed
eagle (Haliaeetus albicilla), 2 giffon vultures (Gyps ful-
vus), 1 sparrow hawk (Accipiter nisus), 4 lesser kestrels
(Falco naumanni), 1 kestrel (Falco tinnunculus), 3 Euro-
pean sparrows (Passer domesticus), 13 rooks (Corvus
frugilegus), 3 jackdaws (Corvus monedula), 4 whooper
swans (Cygnus cygnus), 3 white storks (Ciconia ciconia),
1 capercaillie (Tetrao urogallus) and 1 starling (Sturnus
vulgaris). Fecal samples from 107 free-living birds rep-
resenting 25 different species were cultured for Cam-
pylobacter and Salmonella species upon arrival at
rehabilitation centers in Croatia from March 2000–July
2003. The specimens were heterogeneous in sex and age.
Samples of cloacal swabs were collected individually
from each bird.
Bacteriological methods
For the bacteriology, 107 cloacal swabs and droppings
from captured birds were used. Campylobacter isolation
was conducted according to standard procedures fol-
lowing an enrichment period of 24 h at 42 C under
micro-aerobic conditions in a CampyPak Plus micro-
aerophilic system with a palladium catalyst. Cultivation
was performed by plating each sample onto Skirrow
agar. Plates were incubated for 48 h under the same
conditions described above. Suspected colonies were
identified morphologically (Gram stain), biochemically
(oxidase, catalase, sensitivity to nalidixic acid and
cephalotin, hippurate hydrolysis) and biotyped by API
Campy (Linor 1984).
Fresh feces samples and cloacal swabs for Salmonella
isolation were cultured in tetrathionate broth incubated
at 37 C and 42 C, respectively, for 24 h immediately
after collection. A loopful from these broth cultures was
then streaked onto Salmonella-Shigella agar plates and
incubated at 37 C for 24–48 h. Feces samples and clo-
acal swabs were also cultivated on semisolid media
according to Chau-Huang, incubated for 48 h at 42 C,
and then applied to Salmonella-Shigella media. Colonies
suspected of harboring Salmonella were identified mor-
phologically, then biochemically and serologically
according to the Kauffman scheme (Kauffman 1975;
WHO 2001). The slide agglutination test used polyvalent
and monovalent (O) and (H) antisera (Edwards and
Ewing 1972).
Immunochromatographic test for chlamydial antigen
detection
The commercially available Clearview test (Unipath,
Bedford, UK), approved for the direct detection of
Chlamydophila antigen in endocervical swab specimens,
was used for the detection of Chlamydophila sp. in clo-
acal swabs of free-living bird species (Vanrompay et al.
1994; Trap et al. 1994).
 129

Table 1 Isolation rates of

Campylobacter jejuni and Families and species No. of positive reactions/No. of samples tested
Salmonellaspecies from wild
birds in Croatia C. jejuni S. enteriditis S. tiphimurium

Columbidae
Feral pigeon (Columba livia var. domestica) 2/14 0/14 2/14
Laridae
Black-headed gull (Larus ridibundus) 0/8 0/8 1/8
Great black-backed gull (Larus marinus) 0/1 0/1 0/1
Tytonidae
Barn owl (Tyto alba) 0/4 0/4 0/4
Strigidae
Long-eared owl (Asio otus) 0/2 0/2 0/2
Tawny owl (Strix aluco) 0/8 1/8 0/8
Eagle owl (Bubo bubo) 0/11 0/11 0/11
Little owl (Athene noctua) 0/4 0/4 0/4
Ural owl(Strix uralensis) 0/1 0/1 0/1
Ardeidae
Bittern (Botaurus stellaris) 0/3 0/3 0/3
Gray heron (Ardea cinerea) 0/1 0/1 0/1
Accipitridae
Northern harrier (Circus cyaneus) 0/1 0/1 0/1
Buzzard (Buteo buteo) 0/12 2/12 0/12
White-tailed eagle (Haliaeetus albicilla) 0/1 0/1 0/1
Griffon vulture (Gyps fulvus) 0/2 0/2 0/2
Sparrowhawk (Accipiter nisus) 0/1 0/1 0/1
Falconidae
Lesser kestrel (Falco naumanni) 0/4 0/4 0/4
Kestrel (Falco tinnunculus) 0/1 0/1 0/1
Ploceidae
European sparrow (Passer domesticus) 0/3 0/3 0/3
Corvidae
Rook (Corvus frugilegus) 0/13 1/13 1/13
Jackdaw (Corvus monedula) 0/3 0/3 0/3
Anatidae
Whooper swan (Cygnus cygnus) 0/4 0/4 0/4
Ciconiidae
White stork (Ciconia ciconia) 0/3 0/3 0/3
Phasianidae
Capercaillie (Tetrao urogallus) 0/1 0/1 0/1
Sturnidae
Starling (Sturnus vulgaris) 0/1 0/1 0/1
Total 2/107 4/107 4/107

Isolation trials of chlamydiae in eggs

Cloacal swabs that were positive for the Clearview test
were tested by standard procedure on chicken embryos
for the isolation of chlamydiae. Eggs (6–8 days old) that
were free of specific pathogens were inoculated with
0.2 ml of undiluted fecal suspension by the yolk-sac
route. The cloacal swab suspension had been centrifuged
for 15 min at approximately 800·g. The supernatant
was collected for inoculation in chicken embryos; anti-
biotics (streptomycin, kanamycin and vancomycin) were
added. Inoculated embryos were incubated at 37 C.
The yolk sac and allantoic and amniotic fluids were
harvested from embryos that had died 3–9 days post
inoculation. In the embryos that survived, the yolk sacks
were used for blind passages. After 48–72h of incuba-
tion, the yolk sac, allantoic and amniotic fluids were
stained by the Gimenez method (OIE 1996) or prepared
and examined by fluorescent antibody procedures
(Chlamydia Direct IF Identification, BioMerieux,
France) (Daft et al. 2000).
Results
Campylobacter jejuni-like organisms (in following text
termed C. jejuni) were isolated from 2 of 107 free-living
bird species examined (1.9%). Salmonella was isolated
from 8 fecal or cloacal swabs from free-living bird spe-
cies (7.4%). These isolates were identified as S. ty-
phimurium in 4 (3.7%), and S. enteriditis in 4 (3.7%)
free-living birds (Table 1). Chlamydophila sp. was
detected in 3 (2.8%) of 107 tested free-living birds using
only the Clearview test. Chlamydophila sp. was not
isolated from chicken embryos.
Discussion and conclusions
Results of our study indicate that the prevalence of
Campylobacter jejuni (1.9%) and Salmonella sp. (7.4%) is
low in the free-living bird population in the investigated
area. Our data set was composed of many different
130
species, but the number of tested individual birds for each
species was high in some cases (Table 1). Earlier studies
have identified certain species such as feral pigeons, in
which the prevalence of Salmonella sp. is sometimes rather
high (7.4–15.4%), and argued that concern should be
strong regarding epidemiologic disease transmission by
these birds (Gregurić et al. 1991; Vučemilo et al. 2003).
The epidemiological role of free-living birds in the per-
sistence and spread of Salmonella and Campylobacter
species is still the subject of numerous studies (Kapperud
and Rosef 1983; Nastasi et al. 1999). The isolation rate of
Campylobacter from pigeons, crows, gulls and other non-
urban birds was higher than the rate reported by Kap-
perud and Rosef (1983) in Norway but slightly lower than
that reported by Gregurić et al. (1991) for the same bird
species from our geographical region. Waterborne out-
breaks of Campylobacter-associated gastroenteritis
involving aquatic birds as a possible contamination
source have been reported by Palmer et al. (1983). In
general, the possibility exists that environmental con-
tamination of surface waters with Campylobacter could be
caused by free-living birds (such as gulls or swans), and
that when these waters are used for recreational purposes
or consumed untreated, a risk to public health might exist.
Other studies have suggested that wild animals such as
sparrows, rodents and flies carry Campylobacters organ-
isms in their intestines (Rosef and Kapperud 1983;
Cabitra et al. 1992; Jones 2001). Campylobacter spp. may
be spread from wild animal reservoirs to the environment
and transmitted to other animals and humans (Jones
2001). In Portugal, Rodrigues et al. (1998) isolated Cam-
pylobacter from 46% of sparrows and 7% of pigeons.
Similar results were obtained in another study in north-
eastern Portugal in which Campylobacter was isolated
from 45.5% of sparrows (Cabrita et al. 1992).
In our study, pigeons showed no clinical signs of dis-
ease due to Salmonella. Feral pigeons are important car-
riers and may spread such diseases to other species
(Williams et al. 1978). Salmonella species are highly con-
tagious and need close relationships with the target to be
transmitted successfully. In studies of Croatian free-living
bird populations, we found that black-headed gulls also
may be a reservoir for Salmonella in birds, and that the
birds may be carriers of Salmonella infection while
expressing no obvious disease manifestations. The black-
headed gull is a migratory bird and can transfer strains of
Salmonella from sources outside of Croatia. Our results
suggested that the natural occurrence of Salmonella in
healthy birds in Croatia may be low. Thus, we assume that
it is logical to consider analysing the non-epizootic natural
occurrence of Salmonella in the free-living birds. Data
obtained from many different regions are a prerequisite
for thorough risk assessment of the importance of free-
living birds as carriers of Salmonella.
Chlamydophila sp. was detected using the Clearview
test in 3 (2.8%) of 107 cloacal swabs from free-living bird
species. Chlamydophila sp. was not isolated from chicken
embryos, indicating the occurrence of false-positive
results with this test. When the Clearview test was used
to detect chlamydia in human endocervical specimens
(Arumainayagam et al. 1990) and Chlamydophyla sp. in
ovine fetal membranes and vaginal swabs (Wilsmore and
Davidson 1991), in vaginal swabs from koala bears
(Timms and Wood 1990), and in avian cloacal and con-
junctival swabs (Vanrompay et al. 1994), the occurrence
of false-positive results was also described when com-
pared to the tissue culture method. In contrast to our
earlier study investigating humoral immunity to
Chlamydophila sp. in free-living bird species in Croatia
(Vlahović et al. 1998), where we established Chlamydo-
phila sp. infection in some free-living bird species, in the
current study, chlamydiosis was not found in any of the
examined birds. According to Kaleta and Taday (2003),
the bacterium Chlamyodophila psittaci has a wide host
range, and over 469 different species of birds have been
reported to be susceptible to the infection. Schettler et al.
(2003) also detected the C. psittaci antigen in 74% of the
39 free-living birds of prey using PCR in eastern Ger-
many. Domestic and free-living urban pigeons are often
chronically infected with chlamydia organisms and are the
birds most commonly associated with the transmission of
ornithosis to humans, although this disease has also been
associated with starlings, sparrows, turkeys, ducks and
chickens (Fritzsche and Hürter 1976; Weber et al. 1979;
Gerlach 1994a; Andersen and Vanrompay 2000). Birds
have adapted to the disease and show no symptoms, but
act as carriers, shedding the organisms in their feces,
which later may become airborne as dust. Infection by
chlamydia occurs through the inhalation of particles from
dried feces, feathers, nasal discharge, and conjunctival
secretions. Chlamydia may also cause contamination of
animal and human food and unsafe/unsanitary working
conditions (Weber et al. 1979). Chlamydiosis can be a risk
for personnel working with wildlife (Lüthgen 1978).
In conclusion, we have established that some free-liv-
ing bird species from Croatia such as the feral pigeon
(Columba livia domesticus), rook (Corvus frugilegus),
buzzard (Buteo buteo), black-headed gull (Larus ridibun-
dus) and tawny owl (Strix aluco) can be reservoirs of
Campylobacter and Salmonella species, but not of
Chlamydophila sp. However, the contribution of each
of these identified reservoirs of bacterial species to the
incidence of human infections is still unknown and needs
to be investigated.
Acknowledgements All procedures performed in the study of birds
were consistent with (1) the Directive for the Protection of Verte-
brate Animals used for Experimental and Other Scientific Purposes
(86/609/EEC); (2) statements of the Croatian Association for
Wildlife Environment Protection (AWAP) for handling wild ani-
mals (UP/1-230-02/2022-01/47; 251-02-02/02-5); (3) the Certificate
(Maja Popović) of the course on Laboratory Animal Science and
Experimental Design (Budapest, 1998).
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