B. Ječmenica, A. Humski, L. T. Taylor, B. Šimpraga, F. Krstulović, T. Amšel Zelenika, and L. Jurinović*
Gulls are a group of seabirds distributed worldwide that are an important reservoir of Salmonella spp. Salmonellosis is the second most commonly reported gastrointestinal infection in humans, and understanding the role wild birds have in spreading Salmonella can help to improve the health of humans and domestic animals. The mobility and migration capacity of gulls makes them an interesting group for research given their potential role in spreading pathogens. This paper presents the diversity and prevalence of Salmonella spp. in different gull species caught at a landfill in Zagreb in the winter months over a nine-year period from 2014-2022. In total, 1083 cloacal swabs were sampled from six gull species: Black-headed Gull (Larus ridibundus), Yellow-legged Gull (L. michahellis), Caspian Gull (L. cachinnans), Common Gull (L. canus), Lesser Black-back Gull (L. fuscus) and Herring Gull (L. argentatus). The prevalence of Salmonella was 5.82%, and 16 Salmonella serotypes were identified; S. Typhimurium had the highest prevalence (47.62%) followed by S. Enteritidis (12.69%) and S. Infantis (9.52%). To date, 82 Salmonella serotypes have been isolated in research on gulls in Europe, with S. Typhimurium as the most common, followed by S. Agona and S. Enteritidis. In this study, we found three serotypes not previously reported in gulls, S. Yalding, S. Reading and one with the antigenic formula O:17; H:z10; H:e,n,x,z15 (IIIb).
Key words: gull; Salmonella; wild birds; prevalence; serotype
There is strong interest in researching the epidemiology of pathogenic bacteria in wildlife, especially birds. Many species are natural carriers of bacteria and other microorganisms in their intestinal tract (Refsum et al., 2002; Reed et al., 2003; Pennycott et al., 2006). They can shed bacteria into the environment via faeces, thus spreading them to other animals and humans (Hudson et al., 2000). According to EFSA and ECDC (2021), salmonellosis is the second most commonly reported gastrointestinal infection in humans. A major source of infection for humans comes from poultry, pork, and eggs (EFSA and ECDC, 2021). Understanding the role that wild birds play in spreading these bacteria is important for human and domestic animal health. Research to date has primarily been performed on birds already suspected in the spread of pathogens, either directly to humans or through production farms, particularly those that are opportunistic feeders visiting various potential sites of infection (beaches, landfills, farmyards, fishponds, fish markets, farmland, cities, and water reservoirs) in close vicinity to human settlements (Reed et al., 2003; Antilles et al., 2021; Hubalek, 2021).
Gulls are a widespread group of seabirds of the family Laridae, known to be an important reservoir of Salmonella spp. and other pathogens like Campylobacter spp. (Quessy and Messier, 1992; Wahlström et al., 2003; Kinzelman et al., 2008; Rodríguez et al., 2012; Antilles et al., 2015; Dolejska et al., 2016; Toro et al., 2016; Moré et al., 2017). They are a gregarious species, breeding in colonies of varying size, and roosting and feeding together, especially in winter (Harrison et al., 2021). Their mobility and migration capacity makes them interesting for the potential role in the spread of pathogens. Depending on the species, age, area, food availability and breeding season, they can remain near their colonies (less than 50 km), while during the non-breeding season they can travel hundreds of kilometres from their colonies (Arizaga et al., 2010; Juvaste et al., 2017; Enners et al., 2018; Fijn et al., 2022).
This paper presents the diversity and the prevalence of Salmonella spp. in different gull species caught at a landfill in Zagreb over a nine-year period from 2014–2022 and compares the results with those of other gull studies in Europe.
Materials and methods
In the winter period, from December 2014 to March 2022, gulls were captured using a cannon net at the Zagreb city landfill (45.765 N, 16.025 E). Each caught bird was ringed with steel and plastic rings, aged and identified. During every session, between 20 and 83 individual cloacal swabs were collected for Salmonella analysis.
Detection and isolation of Salmonella strains was performed according to the standard EN ISO 6579-1 method. Briefly, within 24 hours of sampling, swabs were placed in buffered peptone water (bioMérieux, France), and upon completion of 18 ± 2 h incubation at 37ºC, 0.1 mL of the sample was inoculated on three spots of one Modified Semi-solid Rappaport Vassiliadis (Biokar Diagnostics, France) agar plate. This was incubated at 41.5 ± 1ºC for 24 ± 3 h, and for an additional 24 ± 3 hours in case of a negative result. If bacterial growth was observed, one loop from the migration zone was inoculated onto Xylose Lysine Deoxycholate agar (Oxoid Ltd, United Kingdom) and Rambach Chromogen agar (Merck, Germany). After the appropriate incubation time, the selective plating media were checked for the presence of colonies considered to be presumptive Salmonella. The selected, presumptive, colonies were sub-cultured onto Columbia agar (bioMérieux, France) as a non-selective medium for the purpose of further biochemical identification, and serotyping as the combination of these test results indicates whether an isolate belongs to the genus Salmonella. Pure colonies showing typical reactions for Salmonella on media for biochemical confirmation (Triple Sugar Iron agar: alkaline – red, slants and acid – yellow, butts, with gas formation and formation of hydrogen sulphide – blackening of the agar; Urea agar – remains unchanged; Lysine Decarboxylase agar – purple colour of the agar) were also tested for the presence of Salmonella O- and H- antigens by slide agglutination using polyvalent and monovalent antisera. Before the detection of the specific O and H antigens, pure colonies cultured on a non-selective agar medium were checked for auto-agglutination using saline solution.
Only non-auto-agglutinating strains proceeded to the determination of the whole antigen formula. Serotyping was performed according to the CEN ISO/TR 6579-3 using polyvalent and monovalent O and H antisera (Bio Rad, France; Statens Serum Institut, Denmark).
In total, 1083 cloacal swabs were collected from six gull species: Black-headed Gull (Larus ridibundus) (n=753), Yellow-legged Gull (L. michahellis) (n=296), Caspian Gull (L. cachinnans) (n=20), Common Gull (L. canus) (n=11), Lesser Black-back Gull (L. fuscus) (n=2) and Herring Gull (L. argentatus) (n=1). The overall Salmonella prevalence in the period 2014–2022 was 5.82%, with 16 different Salmonella serotypes identified (Tab. 1).
S. Typhimurium had the highest prevalence (47.62%) followed by S. Enteritidis (12.69%) and S. Infantis (9.52%). The species with the highest Salmonella prevalence was the Caspian Gull (15.00%) followed by Black-headed Gull (5.71%) and Yellow-legged Gull (5.41%) while the other three species were not positive for Salmonella, though this is likely due to the small sample size. Black-headed Gulls had the highest number of S. Typhimurium isolates (26) including two with its mono-phase variant (4, 5,12:i:-).
Despite the general interest in the epidemiology of pathogens in wild birds, there is still a great need to better understand how birds are involved in pathogen epidemiology. So far, most research has been conducted on Black-headed and Yellow-legged Gulls, with data collected in breeding colonies or rescue centres. Various prevalence rates of Salmonella positive samples have been recorded for these two species, ranging from 6.28 to 31.08% and 1.33 to 26.26%, respectively (Literák et al., 1992; Ferns and Mudge, 2000; Wahlström et al., 2003; Palmgren et al., 2006; Ramos et al., 2010; Masarikova et al., 2016; Migura-Garcia et al., 2017; Antilles et al., 2021; Ebani et al., 2021; Russo et al., 2021). The literature to date reports the isolation of 82 Salmonella serotypes, and by far the most common was S. Typhimurium, followed by S. Agona and S. Enteritidis. According to EFSA and ECDC (2021), S. Typhimurium is the second most common serotype (after S. Enteritidis) causing infections in humans, and it is mostly related to broilers and pig products while S. Enteritidis is primarily related to broilers.
S. Agona is among the top 20 serotypes causing human infections and is associated with various foods such as sushi, ready-to-eat savoury snacks, and cereal (Killalea et al., 1996; Russo et al., 2013; Thompson et al., 2017; EFSA and ECDC, 2021). In the present study, the S. Typhimurium serotype had the highest prevalence, followed by S. Enteritidis and S. Infantis. S. Infantis is the third most common serotype causing salmonellosis in humans and it is strictly related to broiler sources (EFSA and ECDC, 2021).
According to the research in Europe to date, the present study adds three Salmonella serotypes that were not previously reported in gulls: S. Yalding, S. Reading and S. enterica subsp. diarizonae (IIIb_17:z10:e,n,x,z15).
Considering the large number of Salmonella serotypes found in gulls, it is likely that they become carriers after being infected somewhere in the environment, e.g., at feeding places close to productions farm harbouring Salmonella, or by scavenging at landfills or on sewage (Wahlström et al., 2003; Pennycott et al., 2006; Skov et al., 2008; Masarikova et al., 2016; Antilles et al., 2021). The presence and prevalence of Salmonella serotypes in wild birds generally varies substantially, and most studies are not comparable (Skov et al., 2008) and have not examined Salmonella prevalence in relation to other factors such as season, age, feeding behaviour, movement or environment. As such, systematic studies are required to determine the role these birds have in spreading pathogens. Also, additional molecular methods such as whole genome sequencing could help to unravel the similarities among Salmonella isolates from different sources to pinpoint the origin of infections.
This research was financed by Zagreb City Holding Ltd, Subsidiary Čistoća, Croatia. We would also like to thank the Jaki Dečki ringing group for catching gulls and all volunteers that were participating.
References [… show]
1. ANTILLES N., I. GARCÍA-BOCANEGRA, A. ALBA- CASALS, S. LÓPEZ-SORIA, N. PÉREZ-MÉNDEZ, M. SACO, J. GONZÁLEZ-SOLÍS and M. CERDÀ- CUÉLLARET (2021): Occurrence and antimicrobial resistance of zoonotic enteropathogens in gulls from southern Europe. Sci. Total Environ. 763. 10.1016/j.scitotenv.2020.143018
2. ANTILLES, N., L. GARCIA-MIGURA, K. G. JOENSEN, P. LEEKITCHAROENPHON, F. M. AERESTRUP, M. CERDÀ-CUÉLLARET and R. S. HENDRIKSEN (2015): Audouin’s Gull, a potential vehicle of an extended spectrum ß-lactamase producing Salmonella Agona. FEMS. Microbiol Lett. 362, 1-4. 10.1093/femsle/fnu039
3. ARIZAGA, J., A. HERRERO A. GALARZA J. HIDALGO, A. ALDALUR, J. F. CUADRADO and G. OCIO (2010): First-year Movements of Yellow-legged Gull (Larus michahellis lusitanius) from the Southeastern Bay of Biscay. Waterbirds 33, 444-450. 10.1675/063.033.0403
4. ČÍŽEK, A., M. DOLEJSKÁ, R. KARPÍŠKOVÁ, D. DĚDIČOVÁ and I. LITERÁK (2007): Wild Black-headed Gulls (Larus ridibundus) as an environmental reservoir of Salmonella strains resistant to antimicrobial drugs. Eur. J. Wildl. Res. 53, 55-60 10.1007/s10344-006-0054-2
5. DOLEJSKA, M., M. MASARIKOVA, H. DOBIASOVA, I. JAMBOROVA, R. KARPISKOVA, M. HAVLICEK, C. NICHOLAS, D. PRIDDEL, A. ČIZEK and I. LITERAK (2016): High prevalence of Salmonella and IMP-4-producing Enterobacteriaceae in the Silver Gull on Five Islands, Australia. J. Antimicrob Chemother. 71, 63-70. 10.1093/jac/dkv306
6. EBANI, V. V., L. GUARDONE, F. BERTELLONI, S. PERRUCCI, A. POLI and F. MANCIANTI (2021): Survey on the presence of bacterial and parasitic zoonotic agents in the feces of wild birds. Vet. Sci. 8, 171. 10.3390/vetsci8090171
7. EFSA and ECDC (European Food Safety Authority and European Centre for Disease Prevention and Control) (2021): The European Union One Health 2020 Zoonoses Report. EFSA J. 19, 6971, 324. 10.2903/j.efsa.2021.6971 10.2903/j.efsa.2021.6971
8. ENNERS, L., P. SCHWEMMER, A. M. CORMAN, C. C. VOIGT and S. GARTHE (2018): Intercolony variations in movement patterns and foraging behaviors among Herring Gulls (Larus argentatus) breeding in the eastern Wadden Sea. Ecol. Evol. 8, 7529-7542. 10.1002/ece3.4167
9. FERNS, P. N. and G. P. MUDGE (2000): Abundance, diet and Salmonella contamination of gulls feeding at sewage outfalls. Water Res. 34, 2653-2660 10.1016/ S0043-1354(99)00427-3
10. FIJN, R. C., L. L. GOVERS, D. LUTTEROP, R. P. MIDDELVELD and R. S. A. van BEMMELEN (2022): Evidence of Nocturnal Migration over Sea and Sex- Specific Migration Distance of Dutch Black-Headed Gulls. Ardea 110, 15-29. 10.5253/arde.v110i1.a8
11. HARRISON, P., M. PERROW and H. LARSSON (2021): Seabirds, the New Identification Guide. Lynx. 600.
12. CEN ISO/TR 6579-3:2014. Microbiology of the food chain – horizontal method for the detection, enumeration and serotyping of Salmonella. Part 3: Guidelines for serotyping of Salmonella spp.
13. EN ISO 6579:2003/A1:2008. Microbiology of food and animal feeding stuffs – horizontal methods for the detection of Salmonella spp. Amendment 1: Annex D: Detection of Salmonella spp. in animal faeces and in environmental samples from the primary production stage
14. EN ISO 6579-1:2017. Microbiology of the food chain – Horizontal method for the detection, enumeration and serotyping of Salmonella – Part 1: Detection of Salmonella spp.
15. EN ISO 6579-1:2017/A1:2020. Microbiology of the food chain – Horizontal method for the detection, enumeration and serotyping of Salmonella – Part 1: Detection of Salmonella spp.-Amendment 1 Broader range of incubation temperatures, amendment to the status of Annex D, and correction of the composition of MSRV and SC
16. HUBALEK, Z. (2021): Pathogenic microorganisms associated with gulls and terns (Laridae). J. Vertebr. Biol., 70(3), 1-98 10.25225/jvb.21009
17. HUDSON, C. R., C. QUIST, M. D. LEE, K. KEYES, S. V. DODSON, C. MORALES, S. SANCHEZ, D. G. WHITE and J. J. MAURER (2000): Genetic Relatedness of Salmonella Isolates from Nondomestic Birds in Southeastern United States. J. Clin. Microbiol. 38, 1860-1865. 10.1128/ JCM.38.5.1860-1865.2000
18. JUVASTE, R., E. ARRIERO, A. GAGLIARDO, R. HOLLAND, M. J. HUTTUNEN, I. MUELLER, K. THORUP, M. WIKELSKI, J. HANNILA, M.-L. PENTTINEN and R. WISTBACKA (2017): Satellite tracking of red-listed nominate Lesser Black-Backed Gulls (Larus f. fuscus): Habitat specialization in foraging movements raises novel conservation needs. Glob. Ecol. Conserv. 10, 220-230. 10.1016/j.gecco.2017.03.009
19. KILLALEA, D., L. R. WARD, D. ROBERTS, J. de LOUVOIS, F. SUFI, J. M. STUART, P. G. WALL, M. SUSMAN, M. SCHWIEGER, P. J. SANDERSON, I. S. T. FISHER, P. S. MEAD, N. GILL, C. L. R. BARTLETT and B. ROWE (1996): International epidemiological and microbiological study of outbreak of Salmonella agona infection from a ready to eat savoury snack–II: Israel. BMJ 313, 1105- 1107. 10.1136/bmj.313.7065.1105
20. KINZELMAN, J., S. L. MCLELLAN, A. AMICK, J. PREEDIT, C. O. SCOPEL, O. OLAPADE, S. GRADUS, A. SINGH and G. SEDMAK (2008): Identification of human enteric pathogens in gull feces at Southwestern Lake Michigan bathing beaches. Can. J. Microbiol. 54, 1006-1015. 10.1139/W08-096
21. LITERÁK, I., A. ČÍŽEK and M. HONZA (1992): Examinations of Young Black-headed Gulls (Larus ridibundus) for the Detection of Salmonellae in the Environment. Acta Vet. Brno 61, 141-146. 10.2754/avb199261020141
22. MASARIKOVA, M., I. MANGA, A. ČIZEK, M. DOLEJSKA, V. ORAVCOVA, P. MYSKOVA, R. KARPISKOVA and I. LITERAK (2016): Salmonella enterica resistant to antimicrobials in wastewater effluents and Black-headed Gulls in the Czech Republic. Sci. Total Environ. 542, 102-107. 10.1016/j.scitotenv.2015.10.069
23. MIGURA-GARCIA, L., R. RAMOS and M. CERDÀ- CUÉLLAR (2017): Antimicrobial resistance of Salmonella serovars and Campylobacter spp. Isolated from an opportunistic gull species, Yellow- legged Gull (Larus michahellis). J. Wildl. Dis. 53, 148-152. 10.7589/2016-03-051
24. MORÉ, E., T. AYATS, P. G. RYAN, P. R. NAICKER, K. H. KEDDY, D. GAGLIO, M. WITTEVEEN and M. CERDÀ-CUÉLLAR (2017): Seabirds (Laridae) as a source of Campylobacter spp., Salmonella spp. and antimicrobial resistance in South Africa. Environ. Microbiol. 19, 4164-4176. 10.1111/1462- 2920.13874
25. PALMGREN, H., A. ASPÁN, T. BROMAN, K. BENGTSSON, L. BLOMQUIST, S. BERGSTRÖM, M. SELLIN, R. WOLLIN and B. OLSEN (2006): Salmonella in Black-headed Gulls (Larus ridibundus); prevalence, genotypes and influence on Salmonella epidemiology. Epidemiol Infect. 134, 635-644. 10.1017/S0950268805005261
26. PENNYCOTT, T. W., A. PARK and H. A. MATHER (2006): Isolation of different serovars of Salmonella enterica from wild birds in Great Britain between 1995 and 2003. Vet. Rec. 158, 817-820. 10.1136/ vr.158.24.817
27. QUESSY, S. and S. MESSIER (1992): S. Prevalence of Salmonella spp., Campylobacter spp. and Listeria spp. in Ring-billed Gulls (Larus delawarensis). J. Wildl. Dis. 28, 526-531. 10.7589/0090-3558-28.4.526
28. RAMOS, R., M. CERDÀ-CUÉLLAR, F. RAMÍREZ, L. JOVER and X. RUIZ (2010): Influence of Refuse Sites on the Prevalence of Campylobacter spp. and Salmonella Serovars in Seagulls. Appl. Environ. Microbiol. 76, 3052-3056 10.1128/AEM.02524-09
29. REED, K. D., J. K. MEECE, J. S. HENKEL and S. K. SHUKLA (2003): Migration and Emerging Zoonoses: West Nile Virus, Lyme Disease, Influenza A and Enteropathogens. Clin. Med. Res. 1, 5-12 10.3121/cmr.1.1.5
30. REFSUM, T., E. HEIR, G. KAPPERUD, T. VARDUND and G. HOLSTAD (2002): Molecular Epidemiology of Salmonella enterica Serovar Typhimurium Isolates Determined by Pulsed-Field Gel Electrophoresis: Comparison of Isolates from Avian Wildlife, Domestic Animals, and the Environment in Norway. Appl. Environ. Microbiol. 68, 5600-5606 10.1128/AEM.68.11.5600-5606.2002
31. RODRÍGUEZ, F., J. MORENO, R. ORTEGA, C. MATHIEU, A. GARCÍA, F. CERDA-LEAL and D. GONZÁLEZ-ACUÑA (2012): Evidence for Kelp Gulls (Larus dominicanus) and Franklin’s Gulls (Leucophaeus pipixcan) as carriers of Salmonella by real-time polymerase chain reaction. J. Wildl. Dis. 48, 1105-1108. 10.7589/2012-04-104
32. RUSSO, E. T., G. BIGGERSTAFF, R. M. HOEKSTRA, S. MEYER, N. PATEL, B. MILLER and R. QUICK (2013): Recurrent, Multistate Outbreak of Salmonella Serotype Agona Infections Associated with Dry, Unsweetened Cereal Consumption, United States, 2008. J. Food Prot. 76, 227-230. 10.4315/0362-028X.JFP-12-209
33. RUSSO, T. P., A. PACE, L. VARRIALE, L. BORRELLI, A. GARGIULO, M. POMPAMEO, A. FIORETTI and L. DIPINETO (2021): Prevalence and antimicrobial resistance of enteropathogenic bacteria in Yellow-legged Gulls (Larus michahellis) in southern Italy. Animals 11, 1-9. 10.3390/ani11020275
34. SKOV, M. N., J. J. MADSEN, C. RAHBEK, J. LODAL, J. B. JESPERSEN, J. C. JØRGENSEN, H. H. DIETZ, M. CHRIÉL and D. L. BAGGESEN (2008): Transmission of Salmonella between wildlife and meat-production animals in Denmark. J. Appl. Microbiol. 105, 1558-1568. 10.1111/j.1365-2672.2008.03914.x
35. THOMPSON, C. K., Q. WANG, S. K. BAG, N. FRANKLIN, C. T. SHADBOLT, P. HOWARD, E. J. FEARNLEY, H. E. QUINN, V. SINTCHENKO and K. G. HOPE (2017): Epidemiology and whole genome sequencing of an ongoing point-source Salmonella Agona outbreak associated with sushi consumption in western Sydney, Australia 2015. Epidemiol. Infect. 145, 2062-2071. 10.1017/S0950268817000693
36. TORO, M., P. RETAMAL, S. AYERS, M. BARRETO, M. ALLARD, E. W. BROWN and N. GONZALES- ESCALONAE (2016): Whole-genome sequencing analysis of Salmonella enterica serovar Enteritidis isolates in Chile provides insights into possible transmission between gulls, poultry, and humans. Appl. Environ. Microbiol. 82, 6223-6232 10.1128/AEM.01760-16
37. WAHLSTRÖM, H. E. TYSÉN, E. O. ENGVALL, B. BRÄNDSTRÖM, E. ERIKSSON, T. MÖRNER and I. VÅGSHOLM (2003): Survey of Campylobacter species, VTEC 0157 and Salmonella species in Swedish wildlife. Vet. Rec. 153, 74-80. 10.1136/vr.153.3.74
Raznolikost i prevalencija Salmonella spp. u galebovima ulovljenih na odlagalištu otpada, Zagreb, Hrvatska
Biljana JEČMENICA, mag. oecol. et prot. nat., dr. sc. Andrea HUMSKI, dr. med. vet., znanstvena savjetnica, naslovna docentica, Louie Thomas TAYLOR, mag. biol. exp., dr. sc. Borka ŠIMPRAGA, dr. med. vet., viša znanstvena suradnica, Fani KRSTULOVIĆ, dr. med. vet., mr. spec., stručna savjetnica, dr. sc. Tajana AMŠEL ZELENIKA, dr. med. vet., znanstvena suradnica; dr. sc. Luka JURINOVIĆ, Dipl. Biol., znanstveni suradnik, Hrvatski Veterinarski Institut – podružnica Centar za peradarstvo, Zagreb, Hrvatska
Galebovi su skupina morskih ptica raširenih diljem svijeta koje su važan rezervoar Salmonella spp. Salmoneloza je druga najčešće prijavljena gastrointestinalna infekcija u ljudi i razumijevanje uloge koju divlje ptice imaju u širenju Salmonella spp. može pomoći u poboljšanju zdravlja ljudi i domaćih životinja. Mobilnost i migracijska sposobnost čini galebove vrlo zanimljivom skupinom za istraživanje zbog njihove potencijalne uloge u širenju patogena. Kroz ovaj rad prikazujemo raznolikost i prevalenciju Salmonella spp. kod nekoliko vrsta galebova ulovljenih na odlagalištu otpada tijekom zime u Zagrebu kroz devetogodišnje razdoblje, 2014.-2022. Ukupno je uzorkovano 1083 obrisaka kloake od šest vrsta galebova: riječni galeb (Larus ridibundus), galeb klaukavac (L. michahellis), pontski galeb (L. cachinnans), burni galeb (L. canus), tamnoleđi galeb (L. fuscus) i srebrnasti galeb (L. argentatus). Ukupna prevalencija Salmonella spp. je 5,82 % sa 16 identificiranih serotipova. S. Typhimurium ima najveću zastupljenost (47,62 %), zatim S. Enteritidis (12,69 %) i S. Infantis (9,52 %). Prema istraživanjima prisutnosti serotipova Salmonella spp. u galebova u Europi izolirana su njih 82, a najčešće dokazani je S. Typhimurium, zatim S. Agona i S. Enteritidis. Tijekom ovog istraživanja identificirana su tri serotipa koja ranije nisu izdvojena iz galebova S. Yalding i S. Reading te jedan iz podvrste S. enterica subsp. diarizonae (IIIb_O:17; H:z10; H:e,n,x,z15).
Ključne riječi: galeb, Salmonella, divlje ptice, prevalencija, serotip