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Characterization of Salmonella Typhimurium and its monophasic variant 1,4, [5],12:i:- isolated from different sources

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Abstract

In order to characterize the most commonly detected Salmonella serotypes, we tested 124 isolates of S. Typhimurium and 89 isolates of the monophasic variant of S. Typhimurium (S. 1,4, [5],12:i:-) for their antimicrobial susceptibility by means of the Kirby–Bauer disk-diffusion method, and for the detection of 19 genes (four Phage Markers (g13, Sieb, eat, g8), ten prophage-related virulence genes (gipA, gtgB, nanH, gogB, grvA, sopE, sspH1, sspH2, sodC1, gtgE), and five plasmid-borne virulence genes (spvC, pefA, mig5, rcK, srgA)) by means of PCR-based assays. A total of 213 strains were analyzed from, humans (n = 122), animals (n = 25), food (n = 46), and irrigation water (n = 20). S. Typhimurium isolates showed higher variability, in both their resistance profiles and molecular typing, than S. 1,4, [5],12:i:-. Strains from irrigation water displayed significantly higher susceptibility to antibiotics than those from the other sources. Resistance to ampicillin, streptomycin, sulfonamide, and tetracycline was the most commonly detected resistance profile (R-type), being in serovar S. 1,4, [5],12:i:-, frequently associated to resistance to other antimicrobials. Significant differences in genetic profiles in the two abovementioned Salmonella serotypes were found. None of the plasmid-borne virulence genes investigated were detected in S. 1,4, [5],12:i:- isolates, while those genes, characterized 37.9% of the S. Typhimurium strains. Differences in the prevalence of some molecular targets between the two Salmonella serotypes deserve further study. Importantly, the grvA gene was found exclusively in S. Typhimurium strains, whereas sopE, sodC, gtgB, and gipA were mainly detected, with a statistically significant difference, in S. 1,4, [5],12:i:- isolates.

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References

  • Barco L, Lettini AA, Longo A, Saccardin C, Dalla Pozza MC, Ricci A (2011) A rapid and sensitive method to identify and differentiate Salmonella enterica serotype Typhimurium and Salmonella enterica serotype 4,[5],12:i:- by combining traditional serotyping and multiplex polymerase chain reaction. Foodborne Pathog Dis 8:741–743

    CAS  PubMed  PubMed Central  Google Scholar 

  • Borriello G, Lucibelli MG, Pesciaroli M, Carullo MR, Graziani C, Ammendola S, Battistoni A, Ercolini D, Pasquali P, Galiero G (2012) Diversity of Salmonella spp. serovars isolated from the intestines of water buffalo calves with gastroenteritis. BMC Vet Res 8:201

    PubMed  PubMed Central  Google Scholar 

  • Brendan R, Jackson P, Griffin M, Cole D, Kelly A, Walsh, Chai SJ (2013) Outbreak associated Salmonella enterica serotypes and food commodities, United States, 1998–2008. Emerg Infect Dis 19:1239–1244

    Google Scholar 

  • Brussow H, Canchaya C, Wolf-Dietrich H (2004) Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68:560–602

    PubMed  PubMed Central  Google Scholar 

  • Capuano F, Mancusi A, Capparelli R, Esposito S, Proroga YTR (2013) Characterization of drug resistance and virulotypes of Salmonella strains isolated from food and humans. Foodborne Pathog Dis 10:963–968

    CAS  PubMed  Google Scholar 

  • Chiu CH, Ou JT (1996) Rapid identification of Salmonella serovars in feces by specific detection of virulence genes, invA and spvC, by an enrichment broth culture-multiplex PCR combination assay. J Clin Microbiol 34:2619–2622

    CAS  PubMed  PubMed Central  Google Scholar 

  • CLSI (2018) Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. In: CLSI supplement VET08, 4th edn. Clinical and Laboratory Standards Institute, Wayne, PA

    Google Scholar 

  • De la Torre E, Zapata D, Tello M, Mejía W, Frías N, García Pena FJ, Mateu EM, Torre E (2003) Several Salmonella enterica subsp. enterica serotype 1,4,[5],12:i:- phage types isolated from swine samples originate from serotype Typhimurium DT U302. J Clin Microbiol 41:2395–2400

    PubMed  PubMed Central  Google Scholar 

  • Dionisi AM, Graziani C, Lucarelli C, Filetici E, Villa L, Owczarek S, Caprioli A, Luzzi I (2009) Molecular characterization of multidrug resistant strains of Salmonella enterica serotype Typhimurium and monophasic variant (S. 4,[5],12:i:-) isolated from human infections in Italy. Foodborne Pathog Dis 6:711–717

    CAS  PubMed  Google Scholar 

  • Drahovskà H, Mikasovà E, Szemes T, Ficek A, Sasik M, Majan V, Turna J (2007) Variability in occurrence of multiple prophage genes in Salmonella Typhimurium strains isolated in Slovak Republic. FEMS Microbiol Lett 270:237–244

    PubMed  Google Scholar 

  • EFSA (2010) European food safety authority Panel on Biological Hazards (BIOHAZ). Scientific opinion on monitoring and assessment of the public health risk of "Salmonella Typhimurium-like" strains. EFSA J 8:1826

    Google Scholar 

  • EFSA ECDC (2014) European food safety authority, european centre for disease prevention and control. The european union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2012. EFSA J 12(2):3547

    Google Scholar 

  • Galan JE, Zhou D (2000) Striking a balance: modulation of the actin cytoskeleton by Salmonella. Proc Natl Acad Sci U S A 97:8754–8761

    CAS  PubMed  PubMed Central  Google Scholar 

  • Golberg D, Kroupitski Y, Belausov E, Pinto R, Sela S (2011) Salmonella typhimurium internalization is variable in leafy vegetables and fresh herbs. Int J Food Microbiol 145:250–257

    PubMed  Google Scholar 

  • Guibourdenche M, Roggentin P, Mikoleit M, Fields P, Bockemühl J, Grimont PA, Weill FX (2010) Supplement 2003-2007 (no. 47) to the white-Kauffmann-Le minor scheme. Res Microbiol 161:26–29

    PubMed  Google Scholar 

  • Guiney DG, Fang FC, Krause M, Libby S (1994) Plasmid-mediated virulence genes in non-typhoid Salmonella serovars. FEMS Microbiol Lett 124:1–9

    CAS  PubMed  Google Scholar 

  • Hanning IB, Nutt JD, Ricke SC (2009) Salmonellosis outbreaks in the United States due to fresh produce: sources and potential intervention measures. Foodborne Pathog Dis 6:635–648

    PubMed  Google Scholar 

  • Hauser E, Tietze E, Helmuth R, Junker E, Blank K, Prager R, Rabsch W, Appel B, Fruth A, Malorny B (2010) Pork contaminated with Salmonella enterica serovar 1,4,[5],12:i:-, an emerging health risk for humans. Appl Environ Microbiol 76:4601–4610

    CAS  PubMed  PubMed Central  Google Scholar 

  • Helms M, Ethelberg S, Mølbak K (2005) International Salmonella Typhimurium DT104 infections, 1992–2001. Emerg Infect Dis 11:859–867

    PubMed  PubMed Central  Google Scholar 

  • Ho TD, Slauch JM (2001) Characterization of grvA, an antivirulence gene on the gifsy-2 phage in Salmonella enterica serovar Typhimurium. J Bacteriol 83:611–620

    Google Scholar 

  • Ho TD, Figueroa Bossi N, Wang M, Uzzau S, Bossi L, Slauch JM (2002) Identification of GtgE, a novel virulence factor encoded on the Gifsy-2 bacteriophage of Salmonella enterica serovar Typhimurium. J Bacteriol 184:5234–5239

    CAS  PubMed  PubMed Central  Google Scholar 

  • Holley RA, Arrus KM, Ominski KH, Tenuta M, Blank G (2006) Salmonella survival in manure-treated soils during simulated seasonal temperature exposure. J Environ Qual 31(35):1170–1180

    Google Scholar 

  • Islam M, Morgan J, Doyle MP, Phatak SC, Millner P, Jiang XP (2004) Fate of Salmonella enterica serovar Typhimurium on carrots and radishes grown in fields treated with contaminated manure composts or irrigation water. Appl Environ Microbiol 70:2497–2502

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jiménez L, Muñiz I, Toranzos GA, Hazen TC (1989) Survival and activity of Salmonella Typhimurium and Escherichia coli in tropical freshwater. J Appl Bacteriol 67:61–69

    PubMed  Google Scholar 

  • Lan R, Reeves PR, Octavia S (2009) Population structure, origins and evolution of major Salmonella enterica clones. Infect Genet Evol 9:996–1005

    CAS  PubMed  Google Scholar 

  • Lucarelli C, Dionisi AM, Torpdah M, Villa L, Graziani C, Hopkins K, Threlfall J, Caprioli A, Luzzi I (2010) Evidence for a second genomic island conferring multidrug resistance in a clonal group of strains of Salmonella enterica serovar Typhimurium and its monophasic variant circulating in Italy, Denmark, and the United Kingdom. J Clin Microbiol 48:2103–2109

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mikasovà E, Drahovska H, Szemes T, Kuchta T, Karpiskova R, Sasik M, Turna J (2005) Characterization of Salmonella enterica serovar Typhimurium strains of veterinary origin by molecular typing methods. Vet Microbiol 109:113–120

    PubMed  Google Scholar 

  • Mirold S, Rabsch W, Rohde M, Stender S, Tschäpe H, Rüssmann H, Igwe E, Hardt WD (1999) Isolation of a temperate bacteriophage encoding the type III effector protein sopE from an epidemic Salmonella Typhimurium strain. Proc Natl Acad Sci U S A 96:9845–9850

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moore BC, Martinez E, Gay JM, Rice DH (2003) Survival of Salmonella enterica in freshwater and sediments and transmission by the aquatic midge Chironomus tentans (Chironomidae: Diptera). Appl Environ Microbiol 69(8):4556–4560

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mossong J, Marques P, Ragimbeau C, Huberty Krau P, Losch S, Meyer G, Moris G, Strottner C, Rabsch W, Schneider F (2007) Outbreaks of monophasic Salmonella enterica serovar 4,[5],12:i:- in Luxembourg, 2006. Euro Surveill 12:156–158

    Google Scholar 

  • Petrovska L, Mather AE, AbuOun M, Branchu P, Harris SR, Connor T, Hopkins KL, Underwood A, Lettini AA, Page A, Bagnall M, Wain J, Parkhill J, Dougan G, Davies R, Kingsley RA (2016) Microevolution of monophasic Salmonella Typhimurium during epidemic, United Kingdom, 2005–2010. Emerg Infect Dis 22:617–624

    CAS  PubMed  PubMed Central  Google Scholar 

  • Proroga YTR, Capuano F, Carullo MR, La Tela I, Capparelli R, Barco L, Pasquale V (2016) Occurrence and antimicrobial resistance of Salmonella strains from food of animal origin in southern Italy. Folia Microbiol 61:21–27

    CAS  Google Scholar 

  • Proroga YTR, Capuano F, Capparelli R, Bilei S, Bernardo M, Cocco MP, Campagnuolo R, Pasquale V (2018) Characterization of non-typhoidal Salmonella enterica strains of human origin in central and southern Italy. Ital J Food Saf 7:6888

    PubMed  PubMed Central  Google Scholar 

  • Rahman H, Hardt WD, Murugkar HV, Bhattacharyya DK (2005) Occurrence of sopE gene and its phenotypic expression among different serovars of Salmonella enterica isolated from man and animals. Indian J Exp Biol 43:631–634

    CAS  PubMed  Google Scholar 

  • RAPPORTI ISTISAN15/33 Graziani C, Arigoni F, Turno P, Macchioni D, Pileggi C, Pavia M, Veltri P, Casalinuovo F, Capuano F, Sarnelli P, Luzzi I, Busani L (2015) Valutazione del rischio sanitario di infezioni da agenti zoonosici attraverso prodotti vegetali ottenuti in aree ad elevata pressione zootecnica. v, 98 p. available from 29–10-2015, updated 06–11-2015. http://www.iss.it/binary/publ/cont/15_33_web.pdf

  • Raybaudi Massilia RM, MosquedaMelgar J, Martín Belloso O (2009) Control of pathogenic and spoilage microorganisms in fresh-cut fruits and fruit juices by traditional and alternative natural antimicrobials. Compr Rev Food Sci Food Saf 8:157–180

    CAS  Google Scholar 

  • Sungwoo B, Wuertz S (2012) Survival of host-associated bacteroidales cells and their relationship with Enterococcus spp., Campylobacter jejuni, Salmonella enterica serovar Typhimurium, and adenovirus in freshwater microcosms as measured by propidium monoazide-quantitative PCR. Appl Environ Microbiol 78:922–932

    Google Scholar 

  • Szemes T, Vlková B, Minárik G, Drahovská H, Turna J, Celec P (2012) Does phage P22 contribute to resistance of Salmonella to oxidative stress? Med Hypotheses 79:484–486

    CAS  PubMed  Google Scholar 

  • Tennant SM, Diallo S, Levy H, Livio S, Sow SO, Tapia M, Fields PI, Mikoleit M, Tamboura B, Kotloff KL, Nataro JP, Galen JE, Levine MM (2010) Identification by PCR of non-typhoidal Salmonella enterica serovars associated with invasive infections among febrile patients in Mali. PLoS Negl Trop Dis 4:e621

    PubMed  PubMed Central  Google Scholar 

  • Van Der Linden I, Cottyn B, Uyttendaele M, Berkvens N, Vlaemynck G, Heyndrickx M, Maes M (2014) Enteric pathogen survival varies substantially in irrigation water from Belgian lettuce producers. Int J Environ Res Public Health 11:10105–10124

    Google Scholar 

  • Yang X, Wu Q, Zhang J, Huang J, Guo W, Cai S (2015) Prevalence and characterization of monophasic Salmonella serovar 1,4,[5],12:i:- of food origin in China. PLoS One 10:e0137967

    PubMed  PubMed Central  Google Scholar 

  • You YW, Rankin SC, Aceto HW, Benson CE, Toth JD, Dou ZX (2006) Survival of Salmonella enterica serovar Newport in manure and manure-amended soils. Appl Environ Microbiol 79:5777–5783

    Google Scholar 

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Authors and Affiliations

  1. Department of Food and Feed Control; Laboratory of Molecular Biology, Istituto Zooprofilattico Sperimentale del Mezzogiorno, Via salute, 2., 80055, Portici, Naples, Italy

    Yolande Therese Rose Proroga, Andrea Mancusi, Angela Michela Immacolata Montone & Federico Capuano

  2. Department of Veterinary Medicine and Animal Production, University of Naples Federico II, Naples, Italy

    Maria Francesca Peruzy & Federico Capuano

  3. Department of Food and Feed Control, Centro Tipizzazione Salmonelle, Istituto Zooprofilattico Sperimentale del Mezzogiorno, Via salute, 2., 80055, Portici, Naples, Italy

    Maria Rosaria Carullo & Federico Capuano

  4. Department of Agriculture, University of Naples “Federico II”, Portici, Naples, Italy

    Andrea Fulgione

Authors
  1. Yolande Therese Rose Proroga
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  2. Andrea Mancusi
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  3. Maria Francesca Peruzy
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  4. Maria Rosaria Carullo
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  5. Angela Michela Immacolata Montone
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  6. Andrea Fulgione
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  7. Federico Capuano
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Correspondence to Federico Capuano.

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Proroga, Y.T.R., Mancusi, A., Peruzy, M.F. et al. Characterization of Salmonella Typhimurium and its monophasic variant 1,4, [5],12:i:- isolated from different sources. Folia Microbiol 64, 711–718 (2019). https://doi.org/10.1007/s12223-019-00683-6

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