Characterization of Salmonella Typhimurium and monophasic Salmonella Typhimurium isolated in Abruzzo and Molise regions, Italy, from 2012 to 2017


S. Typhimurium
Monophasic S. Typhimurium
Antimicrobial resistance

How to Cite

Sacchini, L., Ricci, L., Zilli, K., Romantini, R., Di Donato, G., Neri, D., Persiani, T., & Di Giannatale, E. (2021). Characterization of Salmonella Typhimurium and monophasic Salmonella Typhimurium isolated in Abruzzo and Molise regions, Italy, from 2012 to 2017. Veterinaria Italiana, 57(4), 297–304. https://doi.org/10.12834/VetIt.2060.12083.1


Salmonellosis is currently the second most common zoonosis in European Union but in the 6-years periods, between 2012 and 2017, there has been a significant decrease trend in the yearly number of infections caused by Salmonella. In Italy, S. Typhimurium and monophasic S. Typhimurium represent the most prevalent serotypes. In this paper, we investigated these two serovars isolated from 2012 to 2017 in Abruzzo and Molise regions. A set of 345 strains isolated from human sporadic cases, surface water, food and animals were collected and analyzed. Monophasic S. Typhimurium strains were found to be resistant to streptomycin, sulfisoxazole, ampicillin, tetracycline and nalidixic acid, while S. Typhimurium isolates showed high levels of resistance to tetracycline, sulfisoxazole and ampicillin. The 5-loci Multilocus Variable-Number Tandem Repeat Analysis (MLVA) identified 88 genotypes (GT), six of which were common for the two serovars. Several MLVA profiles were shared by human and non-human isolates. MLVA had sufficient typing resolution for epidemiological studies of S. Typhimurium but demonstrated poor discriminatory in trace-back study of monophasic S. Typhimurium.



Barco L., Barrucci F., Cortini E., Ramon E., Olsen J.E., Luzzi I., Lettini A.A. & Ricci A. 2015. Ascertaining the relationship between Salmonella Typhimurium and Salmonella 4,[5],12:i:- by MLVA and inferring the sources of human salmonellosis due to the two serovars in Italy. Front Microbiol, 6, 301.

Barco L., Lettini,A.A., Ramon E., Longo A., Saccardin C., Pozza M.C.D. & 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.

Barco L., Ramon E., Cortini E., Longo A., Dalla Pozza M.C., Lettini A.A., Dionisi A.M., Olsen J.E. & Ricci A. 2014. Molecular characterization of Salmonella enterica serovar 4,[5],12:i:- DT193 ASSuT strains from two outbreaks in Italy. Foodborne Pathog Dis,11, 138–144.

Best E.L., Hampton M.D., Ethelberg S., Liebana E., Clifton-Hadley F.A. & Threlfall E.J. 2009. Drug-resistant Salmonella Typhimurium DT 120: use of PFGE and MLVA in a putative international outbreak investigation. Microb Drug Resist, 15, 133–138.

Cito F., Baldinelli F., Calistri P., Di Giannatale E., Scavia G., Orsini M., Iannetti S., Sacchini L., Mangone I., Candeloro L., Conte A., Ippoliti C., Morelli D., Migliorati G., Barile N.B., Marfoglia C., Salucci S., Cammà C., Marcacci M., Ancora M., Dionisi A.M., Owczartek S., Luzzi I. & outbreak investigation group. 2016. Outbreak of unusual Salmonella enterica serovar Typhimurium monophasic variant 1,4 [5],12:i:-, Italy, June 2013 to September 2014. Euro Surveill, 21(15), 10.2807/1560-7917.ES.2016.21.15.30194. https://doi.org/10.2807/1560-7917.ES.2016.21.15.30194

Clinical and Laboratory Standards Institute (CLSI). 2017. Performance Standards for Antimicrobial Susceptibility Testing. 27th ed. CLSI supplement M100. Wayne, PA.

Dionisi A.M., 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.

European Centre for Disease Prevention and Control (ECDC). 2011. Laboratory standard operating

procedure for MLVA of Salmonella enterica serotype Typhimurium. ECDC, Stockholm.

European Food Safety Authority (EFSA) and European Centre for Disease Prevention and Control (ECDC). 2018. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA Journal, 16(12), e05500.

European Food Safety Authority (EFSA) and European Centre for Disease Prevention and Control (ECDC). 2019. The European Union One Health 2018 Zoonoses Report. EFSA Journal, 19(2), e06406.

EFSA Panel on Biological Hazards (BIOHAZ). 2010 Scientific Opinion on monitoring and assessment of the public health risk of “Salmonella Typhimurium-like” strains. EFSA Journal, 8, 1826.

EFSA Panel on Biological Hazards (BIOHAZ). 2013. Scientific Opinion on the evaluation of molecular typing methods for major food-borne microbiological hazards and their use for attribution modelling, outbreak investigation and scanning surveillance: Part 1 (evaluation of methods and applications). EFSA Journal,11(12), 3502.

Graziani C., Mughini-Gras L., Owczarek S., Dionisi A., Luzzi I. & Busani L. 2013. Distribution of Salmonella enterica isolates from human cases in Italy, 1980 to 2011. Euro Surveill, 18(27), 20519.

Grimont P.A.D. & Weill F.-X. 2007. Antigenic formulae of the Salmonella serovars. 9th ed. Institut Pasteur, Paris, France.

Hopkins K.L., Maguire C., Best E., Liebana E. & Threlfall E.J. 2007. Stability of multiple-locus variable-number tandem repeats in Salmonella enterica serovar typhimurium. J Clin Microbiol, 45, 3058–3061.

Larsson J.T., Torpdahl M., Petersen R.F., Sorensen G., Lindstedt B.A. & Nielsen E.M. 2009. Development of a new nomenclature for Salmonella typhimurium multilocus variable number of tandem repeats analysis (MLVA). Euro Surveill, 14(15), 19174.

Lucarelli C., Dionisi A.M., Torpdahl 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.

Meakins S., Fisher I.S.T., Berghold C., Gerner-Smidt P., Tschäpe H., Cormican M., Luzzi I., Schneider F., Wannett W. Coia J., Echeita A., Threlfall E.J & Enter-net participants. 2008. Antimicrobial drug resistance in human non typhoidal Salmonella isolates in Europe 2000-2004: a report from the Enter-net International Surveillance Network. Microb Drug Resist, 14, 31–35.

Mølbak K., Simonsen J., Jørgensen C.S., Krogfelt K.A., Falkenhorst G., Ethelberg S., Takkinen J. & Emborg HD.2014. Seroincidence of human infections with nontyphoid Salmonella compared with data from public health surveillance and food animals in 13 European countries. Clin Infect Dis, 59(11),1599-1606.

Mueller-Doblies D., Speed., K.C.R., Kidd S. & Davies R.H. 2018. Salmonella Typhimurium in livestock in GreatBritain – trends observed over a 32-year period. Epidemiol Infect,164 (4), 409-422.

Nadon C.A., Trees E., Ng L.K., Møller Nielsen E., Reimer A., Maxwell N., Kubota K.A. & Gerner-Smidt P. 2013. MLVA Harmonization Working Group Development and application of MLVA methods as a tool for inter-laboratory surveillance. Euro Surveill, 18, 20565.

Petersen R.F., Litrup E., Larsson J.T., Torpdahl M., Sørensen G., Müller L. & Nielsen E.M. 2011. Molecular characterization of Salmonella Typhimurium highly successful outbreak strains. Foodborne Pathog Dis, 8, 655–661.

Petrin S., Longo A., Barco L., Cortini E., Peruzzo A., Antonelli P., Ramon E., Cibin V., Lettini A.A. & Ricci A.2019. Different Resolution Power of Multilocus Variable-Number Tandem Repeat Analysis and Whole-Genome Sequencing in the Characterization of S. 1,4,[5],12:i:- Isolates. Foodborne Pathog Dis, 16, 558–561.

Raguenaud M.E., Le Hello S., Salah S., Weill F.X., Brisabois A., Delmas G. & Germonneau P. 2012. Epidemiological and microbiological investigation of a large outbreak of monophasic Salmonella Typhimurium 4,5,12:i:- in schools associated with imported beef in Poitiers, France, October 2010. Euro Surveill, 17, 20289.

Ross I.L., Davos D.E., Mwanri L., Raupach J. & Heuzenroeder M.W. 2011. MLVA and phage typing as complementary tools in the epidemiological investigation of Salmonella enterica serovar Typhimurium clusters. Curr Microbiol, 62, 1034–1038.

Spratt B.G., Hanage W.P., Li B., Aanensen D.M. & Feil E.J. 2004. Displaying the relatedness among isolates of bacterial species - the eBURST approach. FEMS Microbiol Lett, 241, 129–134.

Switt A.I.M., Soyer Y., Warnick L.D. & Wiedmann M. 2009. Emergence, distribution, and molecular and phenotypic characteristics of Salmonella enterica serotype 4,5,12:i:-. Foodborne Pathog Dis, 6, 407–415.

Torpdahl M., Sørensen G., Lindstedt B.-A. & Nielsen E.M. 2007. Tandem repeat analysis for surveillance of human Salmonella Typhimurium infections. Emerging Infect Dis, 13, 388–395.

Copyright (c) 2022 Veterinaria Italiana