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Letter
Salmonella
in Birds Migrating through Sweden
Jorge Hernandez,*† Jonas Bonnedahl,* Jonas Waldenström,*§¶ Helena
Palmgren,‡ and Björn Olsen*‡¶
*Research Institute for Zoonotic Ecology and Epidemiology (RIZEE), Färjestaden,
Sweden; †Kalmar County Hospital, Kalmar, Sweden; ‡Umeå University, Umeå,
Sweden; §Lund University, Lund, Sweden; and ¶Ottenby Bird Observatory,
Degerhamn, Sweden
Suggested citation for this article: Hernandez
J, Bonnedahl J, Waldenström J, Palmgren H, Olsen B. Salmonella
in birds migrating through Sweden. Emerg Infect Dis [serial online]
2003 Jun [date cited]. Available from: URL: http://www.cdc.gov/ncidod/EID/vol9no6/03-0072.htm
To the Editor: To determine how common Salmonella infection
is in the migrating wild bird population, we considered the biology of
the bacterium and that of its avian hosts. Previous studies have attempted
to determine in which stages wild birds become infected, how infections
are acquired, and how this information should be translated into epidemiologic
risk assessments for human and animal health. For instance, most published
studies originate from small epizootics and are of either dead birds at
feeding stations (1) or infected birds in or around barns
where the livestock has Salmonella infection (2).
This bias has important consequences, as the natural prevalence of Salmonella
in the non-epizootic situation likely is overestimated. Finding infected
birds close to a barn with infected cattle does not prove that transmission
occurred from the birds to the animals. In addition, an epizootic at a
feeding station does not prove that Salmonella normally occurs
in the inflicted bird species, as the birds could have became infected
through proximity to the infected animals, or in the case of the bird
feeder, through feed contaminated from an unknown source. We need baseline
surveillance data on the prevalence of Salmonella in non-epizootic
situations, in healthy bird communities and in different stages of a bird’s
life (e.g., during breeding, molting, and migration), to better understand
Salmonella epidemiology in relation to wild birds.
We focused on the migratory bird fauna of the North Western Palearctic,
where most of the birds migrate south to spend the nonbreeding season
in continental Europe and Africa. In these areas, certain species, such
as gulls, corvids, starlings, and thrushes, may overwinter in agricultural
and urban areas were domestic animals are present. We sampled apparently
healthy birds trapped on active migration at Ottenby Bird Observatory
(56°12'N, 16°24'E), on the southernmost tip of the island Öland, southeast
Sweden, during the migration periods July–November 2001, March–May 2002,
and July–December 2002. We used a standardized trapping and sampling scheme,
previously used at the same site for large-scale screening of Campylobacter
infections in wild birds (3). To apply a random procedure
in selection of species and persons, every 10th bird banded during the
migration periods was sampled for Salmonella spp. We did not sample
recaptured birds previously banded by us.
In total, 2,377 samples from 110 species of migratory birds (1,086 samples
in autumn 2001, 777 in spring 2002, and 514 in autumn 2002) were analyzed
for Salmonella infections. We applied routine procedures for isolation
of putative Salmonella isolates, with enrichment in Rappaport-Vassiliadis
broth and injection into xylose-lysine-desoxycholate (XLD) agar. On this
media, most Salmonella enterica serotype Enterica appears as red
transparent colonies with black centers. Colonies with growth characteristics
of Salmonella were observed in 236 samples, and full phenotypic
identification was performed on these isolates by using standard biochemical
and serologic testing. By using the API system (4), the
isolates were identified as Citrobacter youngae, C. braakii,
C. freundii, Escherichia vulneris, E. coli, Hafnia alvei, Klebsiella pneumoniae
ozaenae, Acinetobacter baumanii , Providencia stuartii/rettgeri, and
Yersinia kristen senii. Only one of the isolates, obtained from
a Mistle Thrush (Turdus viscivorus) and sampled during the spring
migration 2002, carried Salmonella. This isolate was characterized
by serotyping according to the Kauffman-White serotyping scheme (5)
at the reference laboratory of the Swedish Institute for Infectious Disease
Control. The thrush isolate was identified as S. Schleissheim,
a rare Salmonella serotype. Human salmonellosis caused by this
serotype has been previously reported only in Turkey (6).
No reservoir of S. Schleissheim, in animals or in humans, has been
reported in Sweden in the last 10 years covered by the current epidemiologic
records.
The failure to find Salmonella was probably not caused by technical
problems. The sampling methods used, with fecal samples from fresh droppings
or cloacal swabs, are well-established techniques for studying Salmonella
prevalence in birds (2,7,8). The laboratory methods used,
with enrichment in Rappaport-Vassaliadis broth and subsequent culturing
on XLD-agar, are extremely sensitive for detecting Salmonella,
even for samples highly contaminated with other Enterobacteriaceae
(9). Thus, in this large dataset, only one Salmonella
isolate was found, representing a serotype rarely observed in clinical
or veterinary samples. In particular, one serotype, S. Typhimurium
DT40, has been associated with epizootics in wintering passerine birds
(10), but this serotype was not found in any of our samples.
Results from our study indicate that the prevalence of this serotype
in the healthy wild bird population is low. Our dataset was composed of
many different species, but the number of tested individual birds for
each species was low in many cases. Earlier studies have pointed to certain
species (gulls and corvids) in which the prevalence of Salmonella
is sometimes high (2% to 20%), and argued that concern should be strong
about epidemiologic disease transmission with these birds (7,8).
These species have the capability to live in an opportunistic manner in
close proximity to humans and can base their diet on waste products and
garbage. Most bird species, however, have little or no niche overlap with
humans or domesticated animals; virtually no data exists on the occurrence
of Salmonella in this major group of migrating birds during a non-epizootic
situation. Our results suggest that the natural occurrence of Salmonella
in healthy birds during migration in Sweden may be low. Therefore, the
Salmonella incidence is probably also low for most wild bird species.
We suggest that researchers consider analyzing the non-epizootic natural
occurrence of Salmonella in wild birds. Accumulated knowledge from
many different regions, over many years, is a prerequisite for thorough
risk assessment of the importance of Salmonella carriage in wild
birds.
Acknowledgments
We thank Paul D. Haemig for valuable comments.
Financial support was provided by the Health Research
Council of Southeast Sweden (2001–02), the Center for Environmental
Research and the Medical Faculty of Umeå University. This is contribution
no. 188 from the Ottenby Bird Observatory.
Mr. Hernandez is a Ph.D. student at the Research Institute
for Zoonotic Ecology and Epidemiology (RIZEE) and at the Department
of Clinical Microbiology, Kalmar County Hospital, Kalmar, Sweden. His
research focuses on the role of wild birds in Salmonella epidemiology.
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