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International journal of food microbiology2023; 408; 110429; doi: 10.1016/j.ijfoodmicro.2023.110429

Salmonella in horses at slaughter and public health effects in Italy.

Abstract: The study assessed the role of equids at slaughter as faecal carriers of Salmonella enterica and the occurrence of contaminated equid carcasses during the slaughter process in Northern Italy (Emilia-Romagna Region). From June to November 2021, 152 equids (146 horses, 5 donkeys and 1 mule) were tested for Salmonella both in caecal contents and through carcass swabs. Antimicrobial resistance (AMR) of recovered strains was tested against 15 antimicrobials. Salmonella was detected in 3/152 of the caecal contents (2.0 %), while all carcass samples were negative. S. enterica serovars Enteriditis, Typhimurium and Stanleyville were identified. The only AMR isolate was S. Typhimurium with AMR profile AmCStxT. Considering the consumption of raw horse meat (i.e., minced raw meat named "pesto di cavallo" and dried and smoked strips named "sfilacci di cavallo") in different areas of Northern Italy, we also investigated the possible link between horse meat eating and salmonellosis cases in the human population in the same area. Specifically, we compared the Salmonella strains collected during the study with those routinely processed in the laboratory surveillance system for human salmonellosis in Emilia-Romagna (a region with about 4.5 million inhabitants). The comparison was based on whole genome sequencing data through core genome multi-locus sequence typing (cgMLST) used in routine surveillance. A genomic match in cgMLST was found between the strain of S. enterica serovar Enteritidis isolated from a horse caecal content and an enduring outbreak of 17 human cases in Emilia-Romagna during the study period. The consequent epidemiological investigation highlighted that a number of cases with known food history reported the consumption of horse meat and traced different batches of the consumed meat, released weeks apart from each other, to the slaughter investigated in the study. The results of the epidemiological investigation suggested the role of horses in the S. enterica serovar Enteritidis outbreak affecting raw horse meat consumers. This study shows that, despite the low prevalence on equid carcasses, S. enterica in horse meat can represent a risk to consumers. From the perspective of the slaughter activities, this highlights the need to maintain a high level of hygiene during the entire process, starting from the hygiene at lairage up to the slaughtering phase and dressing of carcasses.
Publication Date: 2023-10-05 PubMed ID: 37839149DOI: 10.1016/j.ijfoodmicro.2023.110429Google Scholar: Lookup
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  • Journal Article

Summary

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Overview

  • This study investigated the presence of Salmonella enterica in horses and other equids at slaughter in Northern Italy and assessed the potential public health risk linked to consumption of raw horse meat.
  • The research combined microbiological testing of equid samples with genomic analysis and epidemiological data to explore any connections between Salmonella strains found in horses and human salmonellosis cases in the region.

Study Background and Objectives

  • Salmonella enterica is a significant foodborne pathogen, and identifying animal carriers is important for controlling human infections.
  • Horses and other equids are not common sources of salmonellosis, but raw horse meat consumption in some Italian regions raises potential risks.
  • The study aimed to:
    • Determine the prevalence of Salmonella in caecal contents and carcasses of equids at slaughter.
    • Assess antimicrobial resistance profiles of any Salmonella strains found.
    • Evaluate links between Salmonella isolated from equids and human salmonellosis cases through genomic comparisons.

Methods

  • Sampling Period and Location: June to November 2021 in Emilia-Romagna, Northern Italy.
  • Sampled Animals: 152 equids, including 146 horses, 5 donkeys, and 1 mule.
  • Testing:
    • Caecal contents collected at slaughter were tested for Salmonella presence.
    • Carcass swabs were taken to assess contamination during slaughtering.
    • Salmonella isolates underwent antimicrobial resistance testing against 15 drugs.
  • Genomic Comparison:
    • Whole genome sequencing and core genome multi-locus sequence typing (cgMLST) were used to compare Salmonella strains from equids and human patients reported in the regional surveillance system.

Key Findings

  • Salmonella prevalence in caecal contents was low: 3 out of 152 (2.0%).
  • No Salmonella contamination was detected on the carcass surfaces after slaughter.
  • Identified Salmonella serovars included Enteritidis, Typhimurium, and Stanleyville.
  • Only one isolate, S. Typhimurium, exhibited antimicrobial resistance with a profile including ampicillin, chloramphenicol, streptomycin, trimethoprim, and tetracycline (AmCStxT).
  • Genomic analysis revealed a direct match between S. Enteritidis from one horse caecal content and an outbreak strain affecting 17 human cases during the study period.
  • Epidemiological investigation linked these human salmonellosis cases to consumption of raw horse meat products (“pesto di cavallo” and “sfilacci di cavallo”) sourced from batches originating at the studied slaughterhouse.

Public Health Implications

  • The study demonstrates that even with low prevalence in equids and no detected carcass contamination post-slaughter, Salmonella in horse meat can cause human outbreaks.
  • Raw horse meat products, popular in some Italian regions, represent a potential foodborne risk due to Salmonella carriage.
  • A genomic match linking equid isolates to human cases underscores the need for integrated surveillance combining animal and human data.

Recommendations for Slaughter Practices and Consumer Safety

  • Maintaining strict hygiene protocols throughout slaughter is critical, including:
    • Proper hygiene at animal lairage (holding areas before slaughter).
    • Careful slaughtering and carcass dressing procedures to prevent cross-contamination.
  • Continuous monitoring and testing of equids at slaughter to detect Salmonella presence and antibiotic resistance.
  • Public health messaging may be necessary to inform consumers about risks associated with raw horse meat consumption.

Conclusions

  • This study highlights horses as potential reservoirs for Salmonella enterica that can lead to human infections, particularly linked to traditional raw horse meat products.
  • It stresses the importance of combining microbiological testing, antimicrobial resistance screening, and genomic epidemiology to understand and mitigate zoonotic risks.
  • Enforcing hygiene in slaughterhouses and awareness among consumers remain key strategies to reduce salmonellosis risks from horse meat.

Cite This Article

APA
Bolzoni L, Conter M, Lamperti L, Scaltriti E, Morganti M, Poeta A, Vecchi M, Paglioli S, Rampini A, Ramoni P, De Vita D, Bacci C, Rega M, Andriani L, Pongolini S, Bonardi S. (2023). Salmonella in horses at slaughter and public health effects in Italy. Int J Food Microbiol, 408, 110429. https://doi.org/10.1016/j.ijfoodmicro.2023.110429

Publication

ISSN: 1879-3460
NlmUniqueID: 8412849
Country: Netherlands
Language: English
Volume: 408
Pages: 110429
PII: S0168-1605(23)00345-8

Researcher Affiliations

Bolzoni, Luca
  • Risk Analysis and Genomic Epidemiology Unit, Istituto Zooprofilattico Sperimentale della Lombardia e dell'Emilia-Romagna, Parma, Italy.
Conter, Mauro
  • Department of Veterinary Science, Unit of Inspection of Food of Animal Origin, University of Parma, Italy.
Lamperti, Luca
  • Department of Veterinary Science, Unit of Inspection of Food of Animal Origin, University of Parma, Italy.
Scaltriti, Erika
  • Risk Analysis and Genomic Epidemiology Unit, Istituto Zooprofilattico Sperimentale della Lombardia e dell'Emilia-Romagna, Parma, Italy.
Morganti, Marina
  • Risk Analysis and Genomic Epidemiology Unit, Istituto Zooprofilattico Sperimentale della Lombardia e dell'Emilia-Romagna, Parma, Italy.
Poeta, Antonio
  • Hygiene and Public Health Unit, Local Health Authority, Reggio Emilia, Italy.
Vecchi, Marco
  • Specialization School in Inspection of Food of Animal Origin, University of Parma, Italy.
Paglioli, Silvia
  • Hygiene and Public Health Unit, Local Health Authority, Parma, Italy.
Rampini, Alessandra
  • Hygiene and Public Health Unit, Local Health Authority, Piacenza, Italy.
Ramoni, Paolo
  • Hygiene and Public Health Unit, Local Health Authority, Piacenza, Italy.
De Vita, Daniela
  • Hygiene and Public Health Unit, Local Health Authority, Reggio Emilia, Italy.
Bacci, Cristina
  • Department of Veterinary Science, Unit of Inspection of Food of Animal Origin, University of Parma, Italy.
Rega, Martina
  • Department of Veterinary Science, Unit of Inspection of Food of Animal Origin, University of Parma, Italy.
Andriani, Laura
  • Department of Veterinary Science, Unit of Inspection of Food of Animal Origin, University of Parma, Italy.
Pongolini, Stefano
  • Risk Analysis and Genomic Epidemiology Unit, Istituto Zooprofilattico Sperimentale della Lombardia e dell'Emilia-Romagna, Parma, Italy.
Bonardi, Silvia
  • Department of Veterinary Science, Unit of Inspection of Food of Animal Origin, University of Parma, Italy. Electronic address: silvia.bonardi@unipr.it.

MeSH Terms

  • Humans
  • Horses
  • Animals
  • Public Health
  • Multilocus Sequence Typing
  • Salmonella Food Poisoning / epidemiology
  • Salmonella enteritidis
  • Salmonella enterica
  • Asteraceae
  • Italy / epidemiology
  • Meat

Conflict of Interest Statement

Declaration of competing interest None.

Citations

This article has been cited 3 times.
  1. Rossi GAM, Sellera FP, Ferraz CM, Carvalho RS, Oliveira APL, Marques CA, Fávaro EBR, Rosa RDS, Silva LAM, Cardozo MV, Stehling EG, Furlan JPR. Antimicrobial-Resistant Enteric Gram-Negative Bacteria Isolated from a Fatal Diarrhea in a Horse: Genomic Characterization of CTX-M-2-Producing Escherichia coli.. Antibiotics (Basel) 2025 Nov 21;14(12).
    doi: 10.3390/antibiotics14121185pubmed: 41463689google scholar: lookup
  2. Tyrnenopoulou P, Tsilipounidaki K, Florou Z, Gkountinoudis CG, Tyropoli K, Starras A, Peleki C, Marneris D, Arseniou N, Lianou DT, Katsarou EI, Petinaki E, Fthenakis GC. Detection of Gastrointestinal Pathogens with Zoonotic Potential in Horses Used in Free-Riding Activities during a Countrywide Study in Greece.. Animals (Basel) 2024 Sep 3;14(17).
    doi: 10.3390/ani14172566pubmed: 39272351google scholar: lookup
  3. Karodia AB, Shaik T, Qekwana DN. Occurrence of Salmonella spp. in animal patients and the hospital environment at a veterinary academic hospital in South Africa.. Vet World 2024 Apr;17(4):922-932.