The epidemiological role of monophasic Salmonella enterica subsp. enterica serovar Typhimurium tends to increase, indicating pandemic spread. The aim of the present study was to confirm the occurrence of this serological variant in Poland and to report the first cases in Belarus and Ukraine. Genetic similarity of monophasic isolates with Salmonella Typhimurium already present in these countries was assessed. Serotyping, duplex–polymerase chain reaction (PCR) assay, antibiotic resistance and pulsed-field gel electrophoresis (PFGE) profiling have been used to meet the study objectives. Monophasic Salmonella Typhimurium was found at low frequency in various sources along the food chain, including feed, animals, meat, and sewage sludge. The first isolates date back to 2008. The clones observed in other European countries were found, along with a number of new, unrelated genetic lineages appearing locally in three countries. Monophasic Salmonella Typhimurium is claimed to replace and discontinue the domination of pentaresistant Salmonella Typhimurium. Pigs and pork are assumed to be the main vectors of monophasic Salmonella Typhimurium, but their relevance for public health is limited.
Get full access to this article
View all access options for this article.
References
1.
BarcoL, LettiniAA, RamonE, LongoA, SaccardinC, PozzaMC, RicciA. 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, 2011; 8:741–743.
2.
BugarelM, GranierSA, BoninE, VignaudML, RousselS, FachP, BrisaboisA. Genetic diversity in monophasic (1,4,[5],12:i:- and 1,4,[5],12:-:1,2) and in non-motile (1,4,[5],12:-:-) variants of Salmonella enterica S. Typhimurium. Food Res Int, 2012; 45:1016–1024.
3.
ChiouCS, HuangJF, TsaiLH, HsuKM, LiaoCS, ChangHL. A simple and low-cost paper-bridged method for Salmonella phase reversal. Diagn Microbiol Infect Dis, 2006; 54:315–317.
4.
CollardJM, BertrandS, DierickK, GodardC, WildemauweC, VermeerschK, DuculotJ, Van ImmerseelF, PasmansF, ImberechtsH, QuinetC. Drastic decrease of Salmonella Enteritidis isolated from humans in Belgium in 2005, shift in phage types and influence on foodborne outbreaks. Epidemiol Infect, 2008; 136:771–781.
5.
DionisiAM, GrazianiC, LucarelliC, FileticiE, VillaL, OwczarekS, CaprioliA, LuzziI. 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, 2009; 6:711–717.
6.
[EFSA] European Food Safety Authority. Analysis of the baseline survey on the prevalence of Salmonella in holdings with breeding pigs in the EU, 2008, Part A: Salmonella prevalence estimates. EFSA J, 2009; 7:1–93.
7.
[EFSA BIOHAZ] EFSA Panel on Biological Hazards. Scientific opinion on monitoring and assesment of public health risk of "Salmonella Typhimurium-like" strains. EFSA J, 2010; 8:1–44.
8.
[EFSA, ECDC] European Food Safety Authority European Centre for Disease Prevention Control. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2009. EFSA J, 2011; 9:1–378.
9.
GaraizarJ, PorwollikS, EcheitaA, RementeriaA, HerreraS, WongRM, FryeJ, UseraMA, McClellandM. DNA microarray-based typing of an atypical monophasic Salmonella enterica serovar. J Clin Microbiol, 2002; 40:2074–2078.
10.
GossnerCM, van CauterenD, Le HelloS, WeillFX, TerrienE, TessierS, JaninC, BrisaboisA, DuschV, VaillantV, Jourdan-da SilvaN. Nationwide outbreak of Salmonella enterica serotype 4,[5],12:i:- infection associated with consumption of dried pork sausage, France, November to December 2011. Euro Surveill, 2012; 17pii=20071.
11.
GrimontPAD, WeillF-X. Antigenic Formulas of Salmonella Serovars, 9th. Paris: WHO Collaborating Centre for Research on Salmonella, Institute Pasteur, 2007.
12.
HauserE, TietzeE, HelmuthR, JunkerE, BlankK, PragerR, RabschW, AppelB, FruthA, MalornyB. Pork contaminated with Salmonella enterica serovar 4,[5],12:i:-, an emerging health risk for humans. Appl Environ Microbiol, 2010; 76:4601–4610.
13.
HopkinsKL, KirchnerM, GuerraB, GranierSA, LucarelliC, PorreroMC, JakubczakA, ThrelfallEJ, MeviusDJ. Multiresistant Salmonella enterica serovar 4,[5],12:i:- in Europe: A new pandemic strain?Euro Surveill, 2010; 15:19580.
14.
LucarelliC, DionisiAM, TorpdahlM, VillaL, GrazianiC, HopkinsK, ThrelfallJ, CaprioliA, LuzziI. 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, 2010; 48:2103–2109.
15.
McQuistonJR, ParrenasR, Ortiz-RiveraM, GheeslingL, BrennerF, FieldsPI. Sequencing and comparative analysis of flagellin genes fliC, fljB, and flpA from Salmonella. J Clin Microbiol, 2004; 42:1923–1932.
16.
MeakinsS, FisherIS, BergholdC, Gerner-SmidtP, TschäpeH, CormicanM, LuzziI, SchneiderF, WannettW, CoiaJ, EcheitaA, ThrelfallEJEnter-net participantsAntimicrobial drug resistance in human nontyphoidal Salmonella isolates in Europe 2000–2004: A report from the Enter-net International Surveillance Network. Microb Drug Resist, 2008; 14:31–35.
17.
MossongJ, MarquesP, RagimbeauC, Huberty-KrauP, LoschS, MeyerG, MorisG, StrottnerC, RabschW, SchneiderF. Outbreaks of monophasic Salmonella enterica serovar 4,[5],12:i:- in Luxembourg, 2006. Euro Surveill, 2007; 12:156–158.
18.
PornruangwongS, SriyapaiT, PulsrikarnC, SawanpanyalertP, BoonmarS, BangtrakulnonthA. The epidemiological relationship between Salmonella enterica serovar typhimurium and Salmonella enterica serovar 4,[5],12:i:- isolates from humans and swine in Thailand. Southeast Asian J Trop Med Public Health, 2008; 39:288–296.
19.
[PZH, GIS] National Institute of Hygiene Chief Sanitary Inspectorate. Infectious Diseases and Poisonings in Poland in 2010. Warsaw, 2011.
20.
RibotEM, FairMA, GautomR, CameronDN, HunterSB, SwaminathanB, BarrettTJ. Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet. Foodborne Pathog Dis, 2006; 3:59–67.
SwittAI, SoyerY, WarnickLD, WiedmannM. Emergence, distribution, and molecular and phenotypic characteristics of Salmonella enterica serotype 4,5,12:i. Foodborne Pathog Dis, 2009; 6:407–415.
23.
TennantSM, DialloS, LevyH, LivioS, SowSO, TapiaM, FieldsPI, MikoleitM, TambouraB, KotloffKL, NataroJP, GalenJE, LevineMM. Identification by PCR of non-typhoidal Salmonella enterica serovars associated with invasive infections among febrile patients in Mali. PLoS Negl Trop Dis, 2010; 4:e621.
24.
Torre de laE, ZapataD, TelloM, MejíaW, FríasN, García PeñaFJ, MateuEM, TorreE. Several Salmonella enterica subsp. enterica serotype 4,5,12:i:- phage types isolated from swine samples originate from serotype typhimurium DT U302. J Clin Microbiol, 2003; 41:2395–2400.
25.
TrupschuchS, Laverde GomezJA, EdiberidzeIet al.Characterisation of multidrug-resistant Salmonella Typhimurium 4,[5],12:i:- DT193 strains carrying a novel genomic island adjacent to the thrW tRNA locus. Int J Med Microbiol, 2010; 300:279–288.
26.
WasylD, SandvangD, SkovMN, BaggesenDL. Epidemiological characteristics of Salmonella Typhimurium isolated from animals and feed in Poland. Epidemiol Infect, 2006; 134:179–185.
27.
ZamperiniK, SoniV, WaltmanD, SanchezS, TheriaultEC, BrayJ, MaurerJJ. Molecular characterization reveals Salmonella enterica serovar 4,[5],12:i:- from poultry is a variant Typhimurium serovar. Avian Dis, 2007; 51:958–964.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
