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In 2016, an outbreak of Typhimurium (STm) with multilocus variable-number tandem repeat analysis (MLVA) profiles historically associated with passerine birds (2-[11-15]-[3-4]-NA-212) occurred among passerines, cats and humans in Sweden. Our retrospective observational study investigated the outbreak and revisited historical data from 2009–16 to identify seasonality, phylogeography and other characteristics of this STm variant. Outbreak isolates were analysed by whole-genome single nucleotide polymorphism (SNP) typing. The number of notified cases of passerine-associated STm among passerines, cats and humans per month and county, and their MLVA profiles, were compared to birdwatchers’ counts of passerines. Seasonal trend decomposition and correlation analysis was performed. Outbreak isolates did not cluster by host on SNP level. Passerine-associated STm was seasonal for birds, cats and humans, with a peak in March. Cases and counts of passerines at bird feeders varied between years. The incidence of passerine-associated STm infections in humans was higher in the boreal north compared with the southern and capital regions, consistent with passerine population densities. Seasonal mass migration of passerines appears to cause STm outbreaks among cats certain years in Sweden, most likely via predation on weakened birds. Outbreaks among humans can follow, presumably caused by contact with cats or environmental contamination.


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  1. Coburn B, Grassl GA, Finlay BB. Salmonella, the host and disease: a brief review. Immunol Cell Biol. 2007;85(2):112-8.  https://doi.org/10.1038/sj.icb.7100007  PMID: 17146467 
  2. Uzzau S, Brown DJ, Wallis T, Rubino S, Leori G, Bernard S, et al. Host adapted serotypes of Salmonella enterica. Epidemiol Infect. 2000;125(2):229-55.  https://doi.org/10.1017/S0950268899004379  PMID: 11117946 
  3. Galán JE. Typhoid toxin provides a window into typhoid fever and the biology of Salmonella Typhi. Proc Natl Acad Sci USA. 2016;113(23):6338-44.  https://doi.org/10.1073/pnas.1606335113  PMID: 27222578 
  4. Rotger R, Casadesús J. The virulence plasmids of Salmonella. Int Microbiol. 1999;2(3):177-84. PMID: 10943411 
  5. Langridge GC, Fookes M, Connor TR, Feltwell T, Feasey N, Parsons BN, et al. Patterns of genome evolution that have accompanied host adaptation in Salmonella. Proc Natl Acad Sci USA. 2015;112(3):863-8.  https://doi.org/10.1073/pnas.1416707112  PMID: 25535353 
  6. Fang FC, Fierer J. Human infection with Salmonella dublin. Medicine (Baltimore). 1991;70(3):198-207.  https://doi.org/10.1097/00005792-199105000-00004  PMID: 2030643 
  7. Hoelzer K, Moreno Switt AI, Wiedmann M. Animal contact as a source of human non-typhoidal salmonellosis. Vet Res (Faisalabad). 2011;42(1):34.  https://doi.org/10.1186/1297-9716-42-34  PMID: 21324103 
  8. Hugas M, Beloeil P. Controlling Salmonella along the food chain in the European Union - progress over the last ten years. Euro Surveill. 2014;19(19):20804.  https://doi.org/10.2807/1560-7917.ES2014.19.19.20804  PMID: 24852953 
  9. Smyser CF, Snoeyenbos GH. A pigeon host-adapted type of Salmonella typhimurium var. Copenhagen. Avian Dis. 1972;16(2):270-7.  https://doi.org/10.2307/1588791  PMID: 4552673 
  10. Rabsch W, Andrews HL, Kingsley RA, Prager R, Tschäpe H, Adams LG, et al. Salmonella enterica serotype Typhimurium and its host-adapted variants. Infect Immun. 2002;70(5):2249-55.  https://doi.org/10.1128/IAI.70.5.2249-2255.2002  PMID: 11953356 
  11. Handeland K, Refsum T, Johansen BS, Holstad G, Knutsen G, Solberg I, et al. Prevalence of Salmonella typhimurium infection in Norwegian hedgehog populations associated with two human disease outbreaks. Epidemiol Infect. 2002;128(3):523-7.  https://doi.org/10.1017/S0950268802007021  PMID: 12113498 
  12. Daoust PY, Busby DG, Ferns L, Goltz J, McBurney S, Poppe C, et al. Salmonellosis in songbirds in the Canadian Atlantic provinces during winter-summer 1997-98. Can Vet J. 2000;41(1):54-9. PMID: 10642873 
  13. Pennycott TW, Mather HA, Bennett G, Foster G. Salmonellosis in garden birds in Scotland, 1995 to 2008: geographic region, Salmonella enterica phage type and bird species. Vet Rec. 2010;166(14):419-21.  https://doi.org/10.1136/vr.b4761  PMID: 20364008 
  14. Refsum T, Vikøren T, Handeland K, Kapperud G, Holstad G. Epidemiologic and pathologic aspects of Salmonella typhimurium infection in passerine birds in Norway. J Wildl Dis. 2003;39(1):64-72.  https://doi.org/10.7589/0090-3558-39.1.64  PMID: 12685069 
  15. Tauni MA, Osterlund A. Outbreak of Salmonella typhimurium in cats and humans associated with infection in wild birds. J Small Anim Pract. 2000;41(8):339-41.  https://doi.org/10.1111/j.1748-5827.2000.tb03214.x  PMID: 11002934 
  16. Giovannini S, Pewsner M, Hüssy D, Hächler H, Ryser Degiorgis MP, von Hirschheydt J, et al. Epidemic of salmonellosis in passerine birds in Switzerland with spillover to domestic cats. Vet Pathol. 2013;50(4):597-606.  https://doi.org/10.1177/0300985812465328  PMID: 23125146 
  17. Taylor DJ, Philbey AW. Salmonella infections in garden birds and cats in a domestic environment. Vet Rec. 2010;167(1):26-7.  https://doi.org/10.1136/vr.c3156  PMID: 20605956 
  18. Marks SL, Rankin SC, Byrne BA, Weese JS. Enteropathogenic bacteria in dogs and cats: diagnosis, epidemiology, treatment, and control. J Vet Intern Med. 2011;25(6):1195-208.  https://doi.org/10.1111/j.1939-1676.2011.00821.x  PMID: 22092607 
  19. Mather AE, Lawson B, de Pinna E, Wigley P, Parkhill J, Thomson NR, et al. Genomic Analysis of Salmonella enterica Serovar Typhimurium from Wild Passerines in England and Wales. Appl Environ Microbiol. 2016;82(22):6728-35.  https://doi.org/10.1128/AEM.01660-16  PMID: 27613688 
  20. Public Health Agency (PHA). Salmonellainfektion. [Salmonellosis]. Solna: PHA. [Accessed: 4 Aug 2019]. Swedish. Available from: https://www.folkhalsomyndigheten.se/folkhalsorapportering-statistik/statistikdatabaser-och-visualisering/sjukdomsstatistik/salmonellainfektion/?t=county&base=domestic.
  21. BirdLife Sverige. [BirdLife Sweden]. Vinterfåglar in på knuten – statistik. [Winter birds around the corner – statistics]. BirdLife Sverige. [Accessed 4 Aug 2019]. Swedish. Available from: https://vinterfaglar.se/stats
  22. Agria Animal Insurance. Årsredovisning 2014. [Annual Report 2014]. Stockholm: Agria Djurförsäkring. [Accessed 4 Aug 2019]. Swedish. Available from: https://www.agria.se/om-agria/arsredovisningar/
  23. European Centre for Disease Prevention and Control (ECDC). Laboratory standard operating procedure for MLVA of Salmonella enterica serotype Typhimurium. Version 1.2. Stockholm: ECDC; 2011. Available from: https://ecdc.europa.eu/sites/portal/files/media/en/publications/Publications/1109_SOP_Salmonella_Typhimurium_MLVA.pdf
  24. McClelland M, Sanderson KE, Spieth J, Clifton SW, Latreille P, Courtney L, et al. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature. 2001;413(6858):852-6.  https://doi.org/10.1038/35101614  PMID: 11677609 
  25. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4):357-9.  https://doi.org/10.1038/nmeth.1923  PMID: 22388286 
  26. Li H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics. 2011;27(21):2987-93.  https://doi.org/10.1093/bioinformatics/btr509  PMID: 21903627 
  27. Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 2006;23(2):254-67.  https://doi.org/10.1093/molbev/msj030  PMID: 16221896 
  28. Sjörs H. Acta Phytogeographica Suecica. [Swedish plant geography - dedicated to Eddy van der Maarel on his 65th birthday. Rydin H, Snoeijs P, Diekmann M, editors.Uppsala: Svenska växtgeografiska sällskapet; 1999. Swedish.
  29. Statistics Sweden (SCB). Statistikdatabasen. [Statistical database]. Stockholm: SCB. [Accessed: 4 Aug 2019]. Swedish. Available from: http://www.statistikdatabasen.scb.se
  30. Statistics Sweden (SCB). Hundar, katter och andra sällskapsdjur 2012. [Dogs, cats and other pets 2012]. Stockholm: SCB; 2013. Swedish. Available from: https://www.skk.se/globalassets/dokument/om-skk/scb-undersokning-hundar-katter-och-andra-sallskapsdjur-2012.pdf
  31. Agresti A, Coull BA. Approximate is Better than "Exact" for Interval Estimation of Binomial Proportions. Am Stat. 1998;52(2):119-26.
  32. Newton I. Advances in the study of irruptive migration. Ardea. 2006;94(3):29.
  33. Eriksson K. Wintering and migration ecology of Siskin (Carduelis spinus) and Redpoll (C. flammea). In: Voous KH, editor. Proceedings of the XVth international ornithological congress; 30 Aug-5 Sep 1970; the Hague, Netherlands. Leiden: E.J. Brill; 1972 p. 642.
  34. McKenzie AJ, Petty SJ, Toms MP, Furness RW. Importance of Sitka Spruce Picea sitchensis seed and garden bird-feeders for Siskins Carduelis spinus and Coal Tits Periparus ater. Bird Study. 2007;54(2):236-47.  https://doi.org/10.1080/00063650709461480 
  35. Svensson S, Svensson M, Tjernberg M. Svensk fågelatlas. [Swedish bird atlas]. Stockholm: Vår Fågelvärld; 1999. Swedish.
  36. Koenig WD, Knops JM. Seed-crop size and eruptions of North American boreal seed-eating birds. J Anim Ecol. 2001;70(4):609-20.  https://doi.org/10.1046/j.1365-2656.2001.00516.x 
  37. Strong C, Zuckerberg B, Betancourt JL, Koenig WD. Climatic dipoles drive two principal modes of North American boreal bird irruption. Proc Natl Acad Sci USA. 2015;112(21):E2795-802.  https://doi.org/10.1073/pnas.1418414112  PMID: 25964328 
  38. BirdLife International. IUCN Red List for birds. BirdLife International. [Accessed: 4 Aug 2019]. Available from: http://datazone.birdlife.org

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