Monophasic Variant of Salmonella Typhimurium 4,[5],12:i:- (ACSSuGmTmpSxt Type) Outbreak in Central Italy Linked to the Consumption of a Roasted Pork Product (Porchetta)

The monophasic variant of S. Typhimurium 4,[5],12:i:- (MVST) is the third most commonly reported Salmonella serovar involved in human infections (8.8%) in the EU and ranks after S. Enteritidis (54.6%) and S. Typhimurium (11.4%). In Italy, in contrast, the MVST has achieved peculiar epidemiological and ecological success which has allowed it to be, since 2011, the serovar most frequently isolated from humans. In the summer of 2022, a foodborne outbreak of the MVST involving 63 people occurred in the Marche Region (Central Italy). A common food exposure source among some human cases was a roasted, ready-to-eat (RTE) pork product, porchetta, which is a typical product of Central Italy. This paper describes the results of investigations conducted to clarify this outbreak. The porchetta was produced by a local manufacturing plant and distributed to at least two local retail stores, one of which was the retail outlet for the manufacturing plant. The MVST was isolated from surface samples collected at the porchetta manufacturing plant and at both local retail stores via bacterial analysis, and the porchetta sampled at one store contained the MVST. These data confirm this type of RTE pork product can be a source of Salmonella infection in humans.

[1]  OECD-FAO Agricultural Outlook 2023-2032 , 2023, OECD-FAO Agricultural Outlook.

[2]  Shifu Chen Ultrafast one‐pass FASTQ data preprocessing, quality control, and deduplication using fastp , 2023, iMeta.

[3]  A. Brisabois,et al.  Countrywide multi-serotype outbreak of Salmonella Bovismorbificans ST142 and monophasic Salmonella Typhimurium ST34 associated with dried pork sausages in France, September to January 2021 , 2023, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[4]  Maria Laura De Marchis,et al.  A Familiar Outbreak of Monophasic Salmonella serovar Typhimurium (ST34) Involving Three Dogs and Their Owner’s Children , 2022, Pathogens.

[5]  Authority European Centre for Disease Prevention Control European Food Safety The European Union One Health 2021 Zoonoses Report , 2022, EFSA journal. European Food Safety Authority.

[6]  Maliha Tahir,et al.  Outbreak of monophasic Salmonella Typhimurium Sequence Type 34 linked to chocolate products , 2022, Annals of medicine and surgery.

[7]  M. Conter,et al.  Prevalence and antimicrobial resistance profile in Salmonella spp. isolates from swine food chain , 2022, Italian journal of food safety.

[8]  G. V. Di Piazza,et al.  Guidelines for reporting Whole Genome Sequencing‐based typing data through the EFSA One Health WGS System , 2022, EFSA Supporting Publications.

[9]  J. Mossong,et al.  Investigation of an international outbreak of multidrug-resistant monophasic Salmonella Typhimurium associated with chocolate products, EU/EEA and United Kingdom, February to April 2022 , 2022, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[10]  Cassandra K. Jones,et al.  Salmonella enterica 4,[5],12:i:- an emerging threat for the swine feed and pork production industry. , 2021, Journal of food protection.

[11]  P. Pasquali,et al.  Occurrence of Salmonella Typhimurium and its monophasic variant (4, [5],12:i:-) in healthy and clinically ill pigs in northern Italy , 2020, Porcine Health Management.

[12]  Honghu Sun,et al.  The Epidemiology of Monophasic Salmonella Typhimurium. , 2020, Foodborne pathogens and disease.

[13]  C. Jernberg,et al.  Outbreak of unusual H2S-negative monophasic Salmonella Typhimurium strain likely associated with small tomatoes, Sweden, August to October 2019 , 2019, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[14]  Yan Li,et al.  Emergence and Dissemination of mcr-Carrying Clinically Relevant Salmonella Typhimurium Monophasic Clone ST34 , 2019, Microorganisms.

[15]  A. Desideri,et al.  A Comparative Genomic Analysis Provides Novel Insights Into the Ecological Success of the Monophasic Salmonella Serovar 4,[5],12:i:- , 2018, Front. Microbiol..

[16]  J. M. Azcona,et al.  Monophasic Salmonella Typhimurium outbreak due to the consumption of roast pork meat , 2018 .

[17]  Fabio Vannucci,et al.  Salmonella enterica Serotype 4,[5],12: i - in Swine in the United States Midwest An Emerging Multidrug-Resistant Clade , 2018, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[18]  Alexandre P. Francisco,et al.  GrapeTree: visualization of core genomic relationships among 100,000 bacterial pathogens , 2017, bioRxiv.

[19]  Mirko Rossi,et al.  chewBBACA: A complete suite for gene-by-gene schema creation and strain identification , 2017, bioRxiv.

[20]  P. Marone,et al.  Foodborne Salmonellosis in Italy: Characterization of Salmonella enterica Serovar Typhimurium and Monophasic Variant 4,[5],12:i- Isolated from Salami and Human Patients. , 2017, Journal of food protection.

[21]  S. Herrera-León,et al.  An outbreak of monophasic and biphasic Salmonella Typhimurium, and Salmonella Derby associated with the consumption of dried pork sausage in Castellon (Spain). , 2016, Enfermedades infecciosas y microbiologia clinica.

[22]  N. Linton,et al.  Notes from the Field: Outbreak of Multidrug-Resistant Salmonella Infections Linked to Pork--Washington, 2015. , 2016, MMWR. Morbidity and mortality weekly report.

[23]  K. Schroder,et al.  Salmonella employs multiple mechanisms to subvert the TLR‐inducible zinc‐mediated antimicrobial response of human macrophages , 2016, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[24]  M. Niederweis,et al.  Mycobacteria, metals, and the macrophage , 2015, Immunological reviews.

[25]  J. Coombes,et al.  Monophasic expression of FliC by Salmonella 4,[5],12:i:- DT193 does not alter its pathogenicity during infection of porcine intestinal epithelial cells. , 2014, Microbiology.

[26]  A. Ricci,et al.  Characterization of an unusual Salmonella phage type DT7a and report of a foodborne outbreak of salmonellosis. , 2014, International journal of food microbiology.

[27]  L. Peixe,et al.  Characterization of the emerging clinically-relevant multidrug-resistant Salmonella enterica serotype 4,[5],12:i:- (monophasic variant of S. Typhimurium) clones , 2014, European Journal of Clinical Microbiology & Infectious Diseases.

[28]  P. Rajala-Schultz,et al.  In-Feed Use of Heavy Metal Micronutrients in U.S. Swine Production Systems and Its Role in Persistence of Multidrug-Resistant Salmonellae , 2014, Applied and Environmental Microbiology.

[29]  J. E. Olsen,et al.  Molecular characterization of Salmonella enterica serovar 4,[5],12:i:- DT193 ASSuT strains from two outbreaks in Italy. , 2014, Foodborne pathogens and disease.

[30]  A. Brisabois,et al.  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. , 2012, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[31]  V. Vaillant,et al.  Nationwide outbreak of Salmonella enterica serotype 4,[5],12:i:- infection associated with consumption of dried pork sausage, France, November to December 2011. , 2012, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[32]  A. Caprioli,et al.  Evidence for a Second Genomic Island Conferring Multidrug Resistance in a Clonal Group of Strains of Salmonellaenterica Serovar Typhimurium and its Monophasic Variant Circulating in Italy, Denmark, and the United Kingdom , 2010, Journal of Clinical Microbiology.

[33]  J. Terajima,et al.  Multiplex polymerase chain reaction assay for selective detection of Salmonella enterica serovar typhimurium. , 2003, Japanese journal of infectious diseases.

[34]  E. Mateu,et al.  Several Salmonella enterica subsp. enterica Serotype 4,5,12:i:− Phage Types Isolated from Swine Samples Originate from Serotype Typhimurium DT U302 , 2003, Journal of Clinical Microbiology.

[35]  E. Borch,et al.  Hazard identification in swine slaughter with respect to foodborne bacteria. , 1996, International journal of food microbiology.

[36]  S A McEwen,et al.  Amplification of an invA gene sequence of Salmonella typhimurium by polymerase chain reaction as a specific method of detection of Salmonella. , 1992, Molecular and cellular probes.

[37]  J. Machado,et al.  Prevalence of Salmonella in chicken carcasses in Portugal. , 1990, The Journal of applied bacteriology.

[38]  H. Belshaw The Food and Agriculture Organization of the United Nations , 1947, International Organization.

[39]  Clinical,et al.  Performance standards for antimicrobial susceptibility testing , 2019 .