Infection dynamics of Salmonella Infantis strains displaying different genetic backgrounds – with or without pESI-like plasmid – vary considerably

References

• Asai T, Itagaki MY, Shiroki Y, et al. Antimicrobial resistance types and genes in Salmonella enterica Infantis isolates from retail raw chicken meat and broiler chickens on farms. J Food Prot. 2006;69:214–216.
   Web of Science ®Google Scholar
• European Food Safety Authority. Eur Union One Health Zoonoses Rep. 2018;17(12):5926.
   Google Scholar
• Duc VM, Nakamoto Y, Fujiwara A, et al. Prevalence of Salmonella in broiler chickens in Kagoshima, Japan in 2009 to 2012 and the relationship between serovars changing and antimicrobial resistance. BMC Vet Res. 2019. doi:https://doi.org/10.1186/s12917-019-1836-6.
   Google Scholar
• Shah DH, Paul NC, Sischo WC, et al. Microbiology and food safety: population dynamics and antimicrobial resistance of the most prevalent poultry-associated Salmonella serotypes. Poult Sci. 2017;96:687–702.
   PubMed Web of Science ®Google Scholar
• Vinuez-Burgos C, Baquero M, Medina J, et al. Occurrence, genotypes and antimicrobial susceptibility of Salmonella collected from broiler production chain within an integrated poultry company. Int J Food Microbiol. 2019. doi:https://doi.org/10.1016/j.ijfoodmicro.2019.03.014.
   Google Scholar
• Vallejos-Sánchez K, Tataje-Lavanda L, Villanueva-Pérez D, et al. Whole-genome sequencing of a Salmonella enterica subsp. enterica serovar Infantis strain isolated from broiler chicken in Peru. Microbiol Resour Announc. 2019;8:e00826–19. doi:https://doi.org/10.1128/MRA.00826-19.
   Web of Science ®Google Scholar
• Bogomazova AN, Gordeeva V, Krylova EV, et al. Mega-plasmid found worldwide confers multiple antimicrobial resistance in Salmonella Infantis of broiler origin in Russia. Int J Food Microbiol. 2020. doi:https://doi.org/10.106/j.ijfoodmicro.2019.108497.
   Web of Science ®Google Scholar
• Gal-Mor O, Valinsky L, Weinberger M, et al. Multidrug-resistant Salmonella enterica serovar Infantis, Israel. Em Infect Dis. 2010;16:1754–1757.
   PubMed Web of Science ®Google Scholar
• Ross IL, Heuzenroeder MW. A comparison of three molecular typing methods for the discrimination of Salmonella enterica serovar Infantis. FEMS Immunol Med Microbiol. 2008;53:375–384.
   PubMedGoogle Scholar
• Gymoese P, Kiil K, Torpdahl M, et al. WGS based study of the population structure of Salmonella enterica serovar Infantis. BMC Genomics. 2019.. doi:https://doi.org/10.1186/s12864-019-6260-6.
   Google Scholar
• Cohen E, Rahav G, Gal-Mor O. Genome sequence of an emerging Salmonella enterica serovar Infantis and genomic comparison with other S. Infantis strains. Genome Biol Evol. 2020;12:223–228.
   Web of Science ®Google Scholar
• Nagy T, Szmolka A, Wilk T, et al. Comparative genome analysis of Hungarian and global strains of Salmonella Infantis. Front Microbiol. 2020;11:539. doi:https://doi.org/10.3389/fmicb.2020.00539.
   Web of Science ®Google Scholar
• Kornschober C, Mitsch P, Pless P, et al. Salmonella Infantis in Austria. Mini-symposium on Salmonella Infantis infections in Poultry. 2019 Oct 10, Vienna, Austria.
   Google Scholar
• Martínez-Puchol S, Riveros M, Ruidias K, et al. Dissemination of a multidrug resistant CTX-M-65 producer Salmonella enterica serovar Infantis clone between marketed chicken meat and children. Int J Food Microbiol. 2021 Feb 23;344:109109. doi:https://doi.org/10.1016/j.ijfoodmicro.2021.109109.
   Web of Science ®Google Scholar
• Aviv G, Tsyba K, Steck N, et al. A unique megaplasmid contributes to stress tolerance and pathogenicity of an emergent Salmonella enterica serovar Infantis strain. Environm Microbiol. 2014;16:977–994.
   Web of Science ®Google Scholar
• Carfora V, Alba P, Leekitcharoenphon P, et al. Colistin resistance mediated by mcr-1 in ESBL-producing, multidrug resistant Salmonella Infantis in broiler chicken industry, Italy (2016-2017). Front Microbiol. 2018;9:1880, doi:https://doi.org/10.3389/fmicb.2018.01880.
   Web of Science ®Google Scholar
• Franco A, Leekitcharoenphon P, Feltrin F, et al. Emergence of clonal lineage of multidrug-resistant ESBL-producing Salmonella Infantis transmitted from broilers and broiler meat to humans in Italy between 2011 and 2014. PLoS One. 2015. doi:https://doi.org/10.1371/journal.pone.0144802.
   Google Scholar
• Nogrady N, Kiraly M, Davies R, et al. Multidrug resistant clones of Salmonella Infantis of broiler origin in Europe. Int J Food Microbiol. 2012. doi:https://doi.org/10.1016/j.ijfoodmicro.2012.04.007.
   Google Scholar
• Alba P, Leekitcharoenphon P, Carfora V, et al. Molecular epidemiology of Salmonella Infantis in Europe: insights into the success of the bacterial host and its parasitic pESI-like megaplasmid. Mol Gen. 2020. doi:https://doi.org/10.1099/Mgen.0.000365.
   Google Scholar
• Kürekci C, Sahin S, Iwan E, et al. Whole-genome sequence analysis of Salmonella Infantis isolated from raw chicken meat samples and insights into pESI-like megaplasmid. Int J Food Microbiol. 2021. doi:https://doi.org/10.1016/j.ijfoodmicro.2020.108956. Epub 2020 Nov 6. PMID: 33189985.
   Google Scholar
• Ortali G. Experiences gathered from the field: hygiene practices and unsolved questions: about recontamination. Mini-Symposium on Salmonella Infantis infections in Poultry. 2019 Oct 10; Vienna.
   Google Scholar
• Pate M, Micunovic J, Golob M, et al. Salmonella Infantis in broiler flocks in Slovenia: The prevalence of multidrug resistant strains with high genetic homogeneity and low biofilm-forming ability. BioMed Res Internat. 2019. doi:https://doi.org/10.1155/2019/4981463.
   Google Scholar
• Pless P, Mitsch P, Schliessnig H. News about the “Salmonella Infantis action plan” in Styria. Mini-Symposium on Salmonella Infantis infections in Poultry. 2019 Oct 10; Vienna.
   Google Scholar
• Drauch V, Ibesich C, Vogl C, et al. In-vitro testing of bacteriostatic and bactericidal efficacy of commercial disinfectants against Salmonella Infantis reveals substantial differences between products and bacterial strains. Int J Food Microbiol. 2020. doi:https://doi.org/10.1016/j.ijfoodmicro.2020.108660.
   Google Scholar
• Eeckhaut V, Haesebrouck F, Ducatelle R, et al. Oral vaccination with a live Salmonella Enteritidis/Typhimurium bivalent vaccine in layers induces cross-protection against caecal and internal organ colonization by a Salmonella Infantis strain. Vet Microbiol. 2018;218:7–12.
   PubMed Web of Science ®Google Scholar
• Camba SI, del Valle FP, Shirota K, et al. Evaluation on 3-week-old layer chicks intratracheally challenged with Salmonella isolates from serogroup c1 (O:6,7) and Salmonella Enteritidis. Avian Pathol. 2020;49:305–310.
   PubMed Web of Science ®Google Scholar
• Hatamzade Isfahani N, Rahimi S, et al. The effect of capsulated and noncapsulated egg-yolk-specific antibody to reduce colonization in the intestine of Salmonella enterica ssp. enterica serovar infantis-challenged broiler chickens. Poult Sci. 2020;99(3):1387–1394. doi:https://doi.org/10.1016/j.psj.2019.11.019.
   Web of Science ®Google Scholar
• SPAdes version 3.11.1 (de novo assembly; GPL v2). Bankevich A, Nurk S, Antipov D, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19:455–477.
   Web of Science ®Google Scholar
• Ridom SeqSphere+ version 7.2 (EULA). Jünemann S, Sedlazeck FJ, Prior K, et al. Updating benchtop sequencing performance comparison. Nat Biotechnol. 2013;31:294–296.
   Web of Science ®Google Scholar
• Yoshida C, Kruczkiewicz P, Laing CR, et al. The Salmonella In Silico Typing Resource (SISTR): an open web-accessible tool for rapidly typing and subtyping draft Salmonella genome assemblies. PLoS ONE ; 11(1):e0147101, doi:https://doi.org/10.1371/journal.pone.0147101.
   Google Scholar
• Whole Genome Alignment from CLC Genomics Workbench version 21.0.3. https://digitalinsights.qiagen.com.
   Google Scholar
• 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.
   Google Scholar
• Paudel S, Hess M, Hess C.  Coinfection of Avibacterium paragallinarum and Gallibacterium anatis in specific-pathogen-free chickens complicate clinical signs of infectious coryza, which can be prevented by vaccination. Avian Dis. 2017;61(1):55–63. doi:https://doi.org/10.1637/11481-081016-Reg.
   PubMed Web of Science ®Google Scholar
• R Core Team version 3.6.1. R A language and environment for statistical computing. R Foundation for statistical computing; 2020; Vienna. Available from: http://www.R-project.org/.
   Google Scholar
• Aviv G, Elpers L, Mikjlin S, et al. The plasmid encoded Ipf and Klf fimbriae display different expression and varying roles in the virulence of Salmonella enterica serovar Infantis in mouse vs. avian hosts. PLoS Pathog. 2017. doi:https://doi.org/10.1371/journal.ppat.1006559.
   Google Scholar
• EFSA (European Food Safety Authority) and ECDC (European Centre for Disease Prevention and Control). The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2017/2018. EFSA Journal. 2020;18(3):166. doi:https://doi.org/10.2903/j.efsa.2020.6007.
   Web of Science ®Google Scholar
• Smith WH, Tucker JF. The virulence of Salmonella strains for chickens: their excretion by infected chickens. J Hyg Camb. 1980;84:479–488.
   PubMedGoogle Scholar
• Berndt A, Wilhelm A, Jugert C, et al. Chicken cecum immune response to Salmonella enterica serovars of different levels of invasiveness. Infect and Immunity. 2007. doi:https://doi.org/10.1128/IAI.00695-07.
   Google Scholar
• Gustafson RH, Kobland JD. Factors influencing salmonella shedding in broiler chickens. J Hyg Camb. 1984;92:385–394.
   Google Scholar
• Heres L, Urlings HAP, Wagenaar JA, et al. Transmission of Salmonella between broiler chickens fed with fermented liquid feed. Epidemiol Infect. 2004. doi:https://doi.org/10.1017/S0950268803001213.
   Google Scholar
• Traub-Dargatz JL, Ladely SR, Dargatz DA, et al. Impact of heat stress on the fecal shedding patterns of Salmonella enterica Typhimurium DT104 and Salmonella enterica Infantis by 5-week-old male broilers. Foodborne Path Dis. 2006;3:178–183.
   PubMed Web of Science ®Google Scholar
• Tellez G, Petrone VM, Escorcia M, et al. Evaluation of avian-specific probiotic and Salmonella Enteritidis-, Salmonella Typhimurium-, and Salmonella Heidelberg-specific antibodies on cecal colonization and organ invasion of Salmonella Enteritidis in broilers. J Food Prot. 2001;64:287–291.
   PubMed Web of Science ®Google Scholar
• Van Immerseel F, De Buck J, Pasmans F, et al. Intermittent long-term shedding and induction of carrier birds after infection of chickens early post-hatch with a low or high dose of Salmonella Enteritidis. Poult Sci. 2004;83(11):1911–1916. doi:https://doi.org/10.1093/ps/83.11.1911.
   PubMed Web of Science ®Google Scholar
• Gast RK, Guard-Bouldin J, Holt PS. The relationship between duration of fecal shedding and the production of contaminated eggs by laying hens infected with strains of Salmonella Enteritidis and Salmonella Heidelberg. Avian Dis. 2005;49(3):382–386. doi:https://doi.org/10.1637/7322-010705R.1.
   PubMed Web of Science ®Google Scholar
• Barrow PA, Bumstead N, Marston K, et al. Faecal shedding and intestinal colonization of Salmonella enterica in in-bred chickens: the effect of host-genetic background. Epidemiol Infect. 2003;132:117–126. doi:https://doi.org/10.1017/S0950268803001274.
   Web of Science ®Google Scholar
• Virlogeux-Payant I, Mompart F, Velge P, et al. Low persistence of a large-plasmid-cured variant of Salmonella Enteritidis in ceca of chicks. Avian Dis. 2003;47:163–168.
   Web of Science ®Google Scholar
• Gast RK, Jones DR, Guraya R, et al. Research note: horizontal transmission and internal organ colonization by Salmonella Enteritidis and Salmonella Kentucky in experimentally infected laying hens in indoor cage-free housing. Poult Sci. 2020;99(11):6071–6074. doi:https://doi.org/10.1016/j.psj.2020.08.006.
   Web of Science ®Google Scholar
• Holden V, Bachmann M. Diverging roles of bacterial siderophores during infection. Metallomics. 2015;7(6):986–995. doi:https://doi.org/10.1039/c4mt00333k.
   Web of Science ®Google Scholar
• Bäumler AJ, Tsolis RM, Bowe FA, et al. The pef fimbrial operon of Salmonella Typhimurium mediates adhesion to murine small intestine and is necessary for fluid accumulation in the infant mouse. Infect and Immun. 1996;64:61–68.
   PubMed Web of Science ®Google Scholar
• Dufresne K, Saulnier-Bellemare J, Daigle F. Functional analysis of the chaperone-usher fimbrial gene clusters of Salmonella enterica serovar typhi. Fron Cell Infect Microbiol; 8:26, doi:https://doi.org/10.3389/fcimb.2018.00026.
   Google Scholar
• Braukmann M, Methner U. Berndt A. immune reaction and survivability of Salmonella Typhimurium and Salmonella Infantis after infection of primary avian macrophages. PLoS ONE. 2015;10(3):e0122540, doi:https://doi.org/10.1371/journal.pone.0122540.
   Web of Science ®Google Scholar
• Aviv G, Cornelius A, Davidovich M, et al. Differences in the expression of SPI-1 genes pathogenicity and epidemiology between the emerging Salmonella enterica serovar Infantis and the model Salmonella enterica serovar Typhimurium. J Infect Dis. 2019;220(6):1071–1081. doi:https://doi.org/10.1093/infdis/jiz235. PMID: 31062854.
   PubMed Web of Science ®Google Scholar
• Kaiser P, Diard M, Stecher B, et al. The streptomycin mouse model for Salmonella diarrhea: functional analysis of the micro-biota, the pathogen’s virulence factors, and the host’s mucosal immune response. Immunol Rev. 2012;245:56–83.
   PubMed Web of Science ®Google Scholar
• Wigley P. Salmonella enterica in the chicken: How it has helped our understanding of immunology in a non-biomedical model species. Front Immunol. 2014;10(5):482, doi:https://doi.org/10.3389/fimmu.2014.00482.
   Google Scholar
• Withanage GS, Wigley P, Kaiser P, et al. Cytokine and chemokine responses associated with clearance of a primary Salmonella enterica serovar Typhimurium infection in the chicken an in protective immunity to rechallenge. Infect Immun. 2005;73(8):5173–5183. doi:https://doi.org/10.1128/IAI.73.8.5173-5182.
   PubMed Web of Science ®Google Scholar
• Berthelot-Herault F, Mompart F, Zygmunt MS, et al. Antibody responses in the serum and gut of chicken lines differing in cecal carriage of Salmonella Enteritidis. Vet. Immunol Immunopathol. 2003;5(96):43–52. doi:https://doi.org/10.1016/s0165-2427(03)00155-7.
   Web of Science ®Google Scholar
• De Vylder J, Dewulf J, Van Hoorebeke S, et al. Horizontal transmission of Salmonella Enteritidis in groups of experimentally infected laying hens housed in different housing systems. Poult Sci. 2011;90(7):1391–1396. doi:https://doi.org/10.3382/ps.2010-00944.
   Web of Science ®Google Scholar