The Current Landscape of Antibiotic Resistance of Salmonella Infantis in Italy: The Expansion of Extended-Spectrum Beta-Lactamase Producers on a Local Scale

Abstract

Salmonella enterica serovar Infantis is one of the five main causes of human salmonellosis in the European Union (EU) and in recent years, has been increasingly reported to carry multiple antimicrobial resistance determinants, including extended-spectrum beta-lactamase (ESBL) genes. In our study, we used WGS-based tools to characterize S. Infantis strains circulating in the Abruzzo and Molise regions of Italy between 2017 and 2020 and compared this local dataset to the S. Infantis population present in Italy over the last two decades. Phylogenetic analyses demonstrated that the majority of strains isolated from poultry and turkeys from Abruzzo and Molise were closely related and belonged to one of the two main genetic clusters present in Italy, which were grouped predominantly as ESBL-producing strains that harbored pESI-like plasmid. We showed that 60% of the local strains carried multiple antibiotic resistance genes, including ESBL gene blaCTX–M–1 as well as aadA1, dfrA1, dfrA14, sul1, and tet(A) genes present on the pESI-like megaplasmid. The analysis of strains from Abruzzo and Molise and the publicly available Italian S. Infantis sequences revealed a dramatic increase in the number of identified AMR genes in the strains isolated after 2011. Moreover, the number of strains resistant to five or more antibiotic classes increased from 20–80% in the last decade likely due to the acquisition of the megaplasmid. The persistence of the ESBL-producing and the multidrug-resistant (MDR) clone of S. Infantis in poultry populations in Italy and in Europe requires rapid and efficient intervention strategies to prevent further expansion of the clone.

Curing of a field strain ofSalmonella entericaserovar Infantis isolated from poultry from its highly stable pESI like plasmid

“…Since its discovery [3, 17], pESI and similar mega-plasmids have been extensively studied and characterized worldwide [4, 10, 12, 19, 20]. These plasmids harbor a wide array of virulence factors, multiple drug resistance genes, various mobile elements, and plasmid maintenance components.…”

Antimicrobial Resistance and Genomic Characterization of Salmonella Infantis from Different Sources

“…The resistances observed in the present study are of particular concern since fluoroquinolones (nalidixic acid and ciprofloxacin) represent the gold standard for treatment against invasive salmonellosis in humans, and ampicillin and tetracycline are widely used in veterinary medicine as first-line treatment in animal infections (Regulation (EU) 2019/6). The latter ones are, along with sulphonamides, the most commonly purchased antimicrobials for veterinary use [ 14 ].…”

“…Interestingly, for S. Infantis, the level of resistance to these antibiotics was higher than the European average, especially for ampicillin (17.4%). The latter differences may be attributed to the fact that Italy is one of the largest consumers of antimicrobials in the EU [ 14 ].…”

“…Antibiotic resistance (AR) plays an important role in the increased incidence of different bacterial infections. Indeed, the high level of resistance and multi-drug resistance (MDR) recorded in S. Infantis in multiple countries (i.e., Italy, Hungary, Germany, Russia, United States) can be considered another reason for the epidemiological success of this serovar [ 13 , 14 ]. The extended AR exhibited by Salmonella species and other pathogenic bacteria is due to the use and misuse of antibiotics in humans and animals (both in livestock and aquaculture species); these latter, moreover, may spread antibiotic-resistant bacteria (ARB) via their faces and contaminate the terrestrial and marine environment [ 12 ].…”

Human Salmonellosis: A Continuous Global Threat in the Farm-to-Fork Food Safety Continuum

“…Outbreak studies have recognized food commodities, including fresh produce, vegetables, cantaloupes, cereals, alfalfa sprouts, fruit/fruit pulp, pistachios, poultry meat, turkeys, tuna, ground beef, pork, dried/shredded coconut, tomatoes, and mangoes, as sources of foodborne Salmonella-related outbreaks in the past decade [16,17]. The magnitude of infection that has been provoked due to antibiotic-resistant variants is recurrently implied as the causative organisms in these outbreaks, resulting in a higher level of systemic diseases, treatment failures, and a surge in hospitalizations [18,19].…”