{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,10]],"date-time":"2026-09-10T00:06:43Z","timestamp":1788998803507,"version":"build-2803163510"},"reference-count":37,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2020,8,24]],"date-time":"2020-08-24T00:00:00Z","timestamp":1598227200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Campylobacteriosis is the most common gastrointestinal bacterial disease in the European Union (EU). Wild birds are one of the natural reservoirs of these pathogens. In this study we tested cloacal swabs of 643 gulls captured on rubbish tip in Zagreb, Croatia for the presence of Campylobacter spp. and found 168 Campylobacter positive samples. We used multilocus sequence typing (MLST) to genotype 62 random C. jejuni isolates from gulls, 24 isolates from broiler caeca, 27 isolates from broiler neck skins and 23 human isolates. Altogether, we identified 44 different STs, from which 19 were newly described. Most of the new STs (14) originate from gulls. Although humans and broilers share the majority of STs and isolates from gulls are separated from these, there was one ST present in all three hosts: 45. Additionally antimicrobial susceptibility to six antimicrobials was performed on 123 C. jejuni strains isolated from broiler caeca (n = 22), neck skins of broilers (n = 20), gulls cloacal swabs (n = 50) and human faeces (n = 31) by the broth microdilution method. Results show lower resistance of gull isolates to NAL and CIP, while resistance to TET was as high as in human and broiler isolates.<\/jats:p>","DOI":"10.3390\/pathogens9090695","type":"journal-article","created":{"date-parts":[[2020,8,24]],"date-time":"2020-08-24T10:37:32Z","timestamp":1598265452000},"page":"695","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Occurrence of Campylobacter jejuni in Gulls Feeding on Zagreb Rubbish Tip, Croatia; Their Diversity and Antimicrobial Susceptibility in Perspective with Human and Broiler Isolates"],"prefix":"10.3390","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6216-3978","authenticated-orcid":false,"given":"Luka","family":"Jurinovi\u0107","sequence":"first","affiliation":[{"name":"Croatian Veterinary Institute, Poultry Centre, Laboratory for Bacteriology, 10000 Zagreb, Croatia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1308-267X","authenticated-orcid":false,"given":"Sanja","family":"Duvnjak","sequence":"additional","affiliation":[{"name":"Croatian Veterinary Institute, Department for Bacteriology and Parasitology, Laboratory for Bacterial Zoonoses and Molecular Diagnostics of Bacterial Diseases, 10000 Zagreb, Croatia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gordan","family":"Kompes","sequence":"additional","affiliation":[{"name":"Croatian Veterinary Institute, Department for Bacteriology and Parasitology, Laboratory for General Bacteriology and Mycology, 10000 Zagreb, Croatia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5413-8393","authenticated-orcid":false,"given":"Silvija","family":"\u0160oprek","sequence":"additional","affiliation":[{"name":"Department of Clinical Microbiology, University Hospital for Infectious Diseases, 10000 Zagreb, Croatia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Borka","family":"\u0160impraga","sequence":"additional","affiliation":[{"name":"Croatian Veterinary Institute, Poultry Centre, Laboratory for Bacteriology, 10000 Zagreb, Croatia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fani","family":"Krstulovi\u0107","sequence":"additional","affiliation":[{"name":"Croatian Veterinary Institute, Poultry Centre, Laboratory for Bacteriology, 10000 Zagreb, Croatia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marina","family":"Mikuli\u0107","sequence":"additional","affiliation":[{"name":"Croatian Veterinary Institute, Department for Veterinary Public Health, Laboratory for Food Microbiology, 10000 Zagreb, Croatia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3027-1306","authenticated-orcid":false,"given":"Andrea","family":"Humski","sequence":"additional","affiliation":[{"name":"Croatian Veterinary Institute, Department for Veterinary Public Health, Laboratory for Food Microbiology, 10000 Zagreb, Croatia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,8,24]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"EFSA, and ECDC (2018). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA J., 16, 10\u201322.","DOI":"10.2903\/j.efsa.2018.5500"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"687","DOI":"10.1128\/CMR.00006-15","article-title":"Global epidemiology of Campylobacter infection","volume":"28","author":"Kaakoush","year":"2015","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1111\/j.1469-185X.2008.00076.x","article-title":"Bacterial pathogens in wild birds: A review of the frequency and effects of infections","volume":"84","author":"Benskin","year":"2009","journal-title":"Biol. Rev. Camb. Philos. Soc."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"3583","DOI":"10.1128\/AEM.02491-07","article-title":"Comparison of Campylobacter population in wild geese with those in starlings and freerange poultry of the same farm","volume":"74","author":"Colles","year":"2009","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"574","DOI":"10.1111\/j.1758-2229.2011.00265.x","article-title":"Campylobacter populations in wild and domesticated Mallard ducks (Anas platyrhynchos)","volume":"3","author":"Colles","year":"2011","journal-title":"Environ. Microbiol. Rep."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"5911","DOI":"10.1128\/AEM.68.12.5911-5917.2002","article-title":"Prevalence of Campylobacter jejuni, Campylobacter lari, and Campylobacter coli in different ecological guilds and taxa of migrating birds","volume":"68","author":"Waldenstrom","year":"2002","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_7","unstructured":"Sheppard, S.K. (2014). Ecology and host association in Campylobacter in wild birds. Campylobacter Ecology and Evolution, Caister Academic Press."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"3196","DOI":"10.1128\/JCM.01086-12","article-title":"A longitudinal 6-year study of the molecular epidemiology of clinical isolates in Oxfordshire UK","volume":"50","author":"Cody","year":"2012","journal-title":"J. Clin. Microbiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"369","DOI":"10.15585\/mmwr.mm6816a2","article-title":"Preliminary incidence and trends of infections with pathogens transmitted commonly through food-Foodborne diseases active surveillance network, 10 U.S. sites, 2015\u20132018","volume":"68","author":"Tack","year":"2019","journal-title":"MMWR. Morb. Mortal. Wkly. Rep."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Havelaar, A.H., Kirk, M.D., Torgerson, P.R., Gibb, H.J., Hald, T., Lake, R.J., Praet, N., Bellinger, D., de Silva, N., and Gargouri, N. (2015). World health organization global estimates and regional comparisons of the burden of foodborne disease in 2010. PLoS Med., 12.","DOI":"10.1371\/journal.pmed.1001923"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"175","DOI":"10.3201\/eid0802.010145","article-title":"Comparative antibiotic resistance in diarrheal pathogens from Vietnam and Thailand, 1996\u20131999","volume":"8","author":"Isenbarger","year":"2002","journal-title":"Emerg. Infec. Dis."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1501","DOI":"10.3201\/eid0812.020115","article-title":"Increasing fluoroquinolone resistance in Campylobacter jejuni, Pennsylvania, USA, 1982\u20132001","volume":"12","author":"Nachamkin","year":"2002","journal-title":"Emerg. Infec. Dis."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1080\/00063650309461291","article-title":"Opportunistic feeding responses of the yellow-legged gull Larus michahellis to accessibility of refuse dumps: The gulls adjust their diet composition and diversity according to refuse dump accessibility","volume":"50","author":"Duhem","year":"2003","journal-title":"Bird Study"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1007\/s10336-008-0346-2","article-title":"Diet of yellow-legged gull (Larus michahellis) chicks along the Spanish Western Mediterranean coast: The relevance of refuse dumps","volume":"150","author":"Ramos","year":"2009","journal-title":"J. Ornithol."},{"key":"ref_15","unstructured":"Ani\u0107 Vu\u010dini\u0107, A. (2012). Dinamika brojnosti i kretanja galebova (Laridae, Aves) koji se hrane na odlagali\u0161tu otpada Prudinec, Zagreb. XII Me\u0111unarodni Simpozij Gospodarenja Otpadom, Geotehni\u010dki Fakultet."},{"key":"ref_16","unstructured":"Kralj, J., Bari\u0161i\u0107, S., \u0106ikovi\u0107, D., and Tuti\u0161, V. (2013). Galeb klaukavac, Larus cachinnans michahellis. Atlas Selidbe Ptica Hrvatske, Hrvatska Akademija Znanosti i Umjetnosti."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"4594","DOI":"10.1128\/JCM.40.12.4594-4602.2002","article-title":"Campylobacter jejuni in Black-Headed Gulls (Larus ridibundus): Prevalence, genotypes, and influence on C. jejuni epidemiology","volume":"40","author":"Broman","year":"2003","journal-title":"J. Clin. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"31","DOI":"10.7589\/2013-06-136","article-title":"Prevalence of three Campylobacter species, C. jejuni, C. coli, and C. lari, using multi locus sequence typing in wild birds of the mid-atlantic region, USA","volume":"50","author":"Keller","year":"2014","journal-title":"J. Wildl. Dis."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1676","DOI":"10.3389\/fmicb.2018.01676","article-title":"Population Structure, antimicrobial resistance, and virulence-associated genes in Campylobacter jejuni isolated from three ecological niches: Gastroenteritis patients, broilers, and wild birds","volume":"9","author":"Guirado","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Griekspoor, P., Hansbro, P.M., Waldenstr\u00f6m, J., and Olsen, B. (2015). Campylobacter jejuni sequence types show remarkable spatial and temporal stability in Blackbirds. Infect. Ecol. Epidemiol., 5.","DOI":"10.3402\/iee.v5.28383"},{"key":"ref_21","first-page":"475","article-title":"Prevalence of thermotolerant Campylobacter spp. in chicken meat in Croatia and multilocus sequence typing of a small subset of Camplobacter jejuni and Campylobacter coli isolates","volume":"54","author":"Humski","year":"2016","journal-title":"Food Techol. Biotechnol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"3404","DOI":"10.1128\/JCM.00042-08","article-title":"Multilocus sequence typing of Campylobacter jejuni isolates from humans, chickens, raw milk, and environmental water in Quebec, Canada","volume":"46","author":"Frost","year":"2008","journal-title":"J. Clin. Microbiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"430","DOI":"10.1186\/s12879-017-2535-1","article-title":"MLST genotypes of Campylobacter jejuni isolated from broiler products, dairy cattle and human Campylobacteriosis cases in Lithuania","volume":"17","author":"Ramonaite","year":"2017","journal-title":"BMC Infect. Dis."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"782","DOI":"10.1111\/1758-2229.12314","article-title":"Wild bird-associated Campylobacter jejuni isolates are a consistent source of human disease, in Oxfordshire, United Kingdom","volume":"7","author":"Cody","year":"2015","journal-title":"Environ. Microbiol. Rep."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Marotta, F., Garofolo, G., di Marcantonio, L., Di Serafino, G., Neri, D., Romantini, R., Sacchini, L., Alessiani, A., di Donato, G., and Nuvoloni, R. (2019). Antimicrobial resistance genotypes and phenotypes of Campylobacter jejuni isolated in Italy from humans, birds from wild and urban habitats, and poultry. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0225231"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"EFSA & ECDC (2020). The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2017\/2018. EFSA J., 18, 6007.","DOI":"10.2903\/j.efsa.2020.6007"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"718","DOI":"10.1128\/CMR.00002-11","article-title":"Food animals and antimicrobials: Impacts on human health","volume":"24","author":"Marshall","year":"2011","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_28","unstructured":"(2017). ECDC\/EFSA\/EMA second joint report on the integrated analysis of the consumption of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from humans and food-producing animals, joint interagency antimicrobial consumption and resistance analysis (JIACRA) Report. EFSA J., 15, 4872."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1377","DOI":"10.3389\/fmicb.2019.01377","article-title":"Overlap of antibiotic resistant Campylobacter jejuni MLST genotypes isolated from humans, broiler products, dairy cattle and wild birds in Lithuania","volume":"10","author":"Aksomaitiene","year":"2019","journal-title":"Front Microbiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"148","DOI":"10.7589\/2016-03-051","article-title":"Antimicrobial resistance of Salmonella serovars and Campylobacter spp. isolated from an opportunistic gull species, yellow-legged gull (Larus michahellis)","volume":"53","author":"Ramos","year":"2017","journal-title":"J. Wildl. Dis."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1111\/zph.12198","article-title":"Antimicrobial resistance and multilocus sequence types of Finnish Campylobacter jejuni isolates from multiple sources","volume":"63","author":"Olkkola","year":"2016","journal-title":"Zoonoses Publ. Health"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Elhadidy, M., Ali, M.M., El-Shibiny, A., Miller, W.G., Elkhatib, W.F., Botteldoorn, N., and Dierick, K. (2020). Antimicrobial resistance patterns and molecular resistance markers of Campylobacter jejuni isolates from human diarrheal cases. PLoS ONE, 15.","DOI":"10.1371\/journal.pone.0227833"},{"key":"ref_33","unstructured":"(2020, June 25). Commission Regulation (EC) No 2073\/2005 of 15 November 2005 on Microbiological Criteria For Foodstuffs, Consolidated Version. Available online: http:\/\/data.europa.eu\/eli\/reg\/2005\/2073\/oj."},{"key":"ref_34","unstructured":"(2020, June 25). Commission Regulation (EC) No 2160\/2003 of the European Parliament and of the Council of 17 November 2003 on the Control of Salmonella and Other Specified Food-Borne Zoonotic Agents Consolidated Version. Available online: http:\/\/data.europa.eu\/eli\/reg\/2003\/2160\/oj."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"4744","DOI":"10.1128\/JCM.40.12.4744-4747.2002","article-title":"Colony multiplex PCR assay for identification and differentiation of Campylobacter jejuni, C. coli, C. lari, C. upsaliensis, and C. fetus subsp. fetus","volume":"40","author":"Wang","year":"2002","journal-title":"J. Clin. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"124","DOI":"10.12688\/wellcomeopenres.14826.1","article-title":"Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications","volume":"3","author":"Jolley","year":"2018","journal-title":"Wellcome Open Res."},{"key":"ref_37","unstructured":"The European Committee on Antimicrobial Susceptibility Testing (2020, June 25). Breakpoint Tables for Interpretation of MICs and Zone Diameters. Version 9.0. Available online: http:\/\/www.eucast.org."}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/9\/9\/695\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T10:06:00Z","timestamp":1760177160000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/9\/9\/695"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,8,24]]},"references-count":37,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2020,9]]}},"alternative-id":["pathogens9090695"],"URL":"https:\/\/doi.org\/10.3390\/pathogens9090695","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,8,24]]}}}