Occurrence and genomic characterization of antimicrobial-resistant and potential pathogenic Escherichia coli from Italian artisanal food productions of animal origin

Published: 25 March 2024
Abstract Views: 186
PDF: 53
SUPPLEMENTARY MATERIAL: 14
HTML: 5
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Authors

Escherichia coli can harbor a broad repertoire of virulence and antimicrobial resistance (AMR) genes, which can be exchanged across the human gastrointestinal microflora, thus posing a public health risk. In this study, 6 batches of artisanal soft cheese and a 6-month ripened fermented dried sausage were investigated to assess the occurrence, phylogeny, and genomic traits (AMR, virulence, and mobilome) of E. coli. 30 and 3 strains isolated from salami and cheese food chains, respectively, were confirmed as E. coli by whole genome sequencing. The accumulation of single nucleotide polymorphism differences within small clusters of strains encompassing batches or processing stages, combined with high serotype and phylogroup diversity, suggested the occurrence of different contamination phenomena among the facilities. A total of 8 isolates harbored plasmid-mediated resistance genes, including one cheese strain that carried an IncQ1 plasmid carrying AMR determinants to macrolides [mph(B)], sulfonamides (sul1, sul2), trimethoprim (dfrA1), and aminoglycosides [aph(3”)-Ib and aph(6)-Id]. A pool of virulence-associated genes in the class of adhesion, colonization, iron uptake, and toxins, putative ColV-positive iron uptake systems sit, iro, or iuc (8 salami and 2 cheese), plasmid-encoded hemolysin operon hlyABCD (one salami), and potential atypical enteropathogenic E. coli (3 salami environment) were reported. Overall, our findings underscore the importance of routine surveillance of E. coli in the artisanal food chain to prevent the dissemination of AMR and virulence.

Dimensions

Altmetric

PlumX Metrics

Downloads

Download data is not yet available.

Citations

Afset JE, Bruant G, Brousseau R, Harel J, Anderssen E, Bevanger L, Bergh K, 2006. Identification of virulence genes linked with diarrhea due to atypical enteropathogenic Escherichia coli by DNA microarray analysis and PCR. J Clin Microbiol 44:3703-11.
Bauer ME, Welch RA, 1996. Characterization of an RTX toxin from enterohemorrhagic Escherichia coli O157: H7. Infect Immun 64:167-75.
Besser J, Carleton HA, Gerner-Smidt P, Lindsey RL, Trees E, 2018. Next-generation sequencing technologies and their application to the study and control of bacterial infections. Clin Microbiol Infect 24:335-41.
Beutin L, 1991. The different hemolysins of Escherichia coli. Med Microbiol Immunol 180:167-82.
Boripun R, Saengsawang P, Intongead S, Narinthorn R, Wongtawan T, Nissapatorn V, de Lourdes Pereira M, Mitsuwan W, 2023. Molecular characterization and nucleotide substitution of antibiotic resistance genes in multidrug-resistant Escherichia coli isolated from environmental swine farms. Emerg Contam 9:100249.
Bryan A, Shapir N, Sadowsky MJ, 2004. Frequency and distribution of tetracycline resistance genes in genetically diverse, nonselected, and nonclinical Escherichia coli strains isolated from diverse human and animal sources. Appl Environ Microbiol 70:2503-7.
Bugarel M, Martin A, Fach P, Beutin L, 2011. Virulence gene profiling of enterohemorrhagic (EHEC) and enteropathogenic (EPEC) Escherichia coli strains: a basis for molecular risk assessment of typical and atypical EPEC strains. BMC Microbiol 11:142.
Clermont O, Bonacorsi S, Bingen E, 2000. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microb 66:4555-8.
Conedera G, Mattiazzi E, Russo F, Chiesa E, Scorzato I, Grandesso S, Bessegato A, Fioravanti A, Caprioli A, 2007. A family outbreak of Escherichia coli O157 haemorrhagic colitis caused by pork meat salami. Epidemiol Infect 135:311-4.
Dalzini E, Cosciani-Cunico E, Bernini V, Bertasi B, Losio MN, Daminelli P, Varisco G, 2015. Behaviour of Escherichia coli O157 (VTEC), Salmonella Typhimurium and Listeria monocytogenes during the manufacture, ripening and shelf life of low fat salami. Food Control 47:306-11.
Denamur E, Clermont O, Bonacorsi S, Gordon D, 2021. The population genetics of pathogenic Escherichia coli. Nat Rev Microbiol 19:37-54.
Dhawde R, Macaden R, Saranath D, Nilgiriwala K, Ghadge A, Birdi T, 2018. Antibiotic resistance characterization of environmental E. coli isolated from river Mula-Mutha, Pune district, India. Int J Environ Res Public Health 15:1247.
Hernandes RT, Elias WP, Vieira MAM, Gomes TAT, 2009. An overview of atypical enteropathogenic Escherichia coli. FEMS Microbiol Lett 297:137-49.
Hussein ND, Hassan JW, Osman M, El-Omari K, Kharroubi SA, Toufeili I, Kassem II, 2023. Assessment of the microbiological acceptability of white cheese (Akkawi) in Lebanon and the antimicrobial resistance profiles of associated Escherichia coli. Antibiotics 12:610.
ISO, 2019. Susceptibility testing of infectious evaluation of performance of antimicrobial susceptibility test devices - Part 1: broth micro-diluition reference method for testing the in vitro activity of antimicrobial agents against rapidly growing aerobic bacteria involved in infectious diseases (second edition). ISO Norm 20776-1:2019. International Standardization Organization ed., Geneva, Switzerland.
Jiang X, Yu T, Wu N, Meng H, Shi L, 2014. Detection of qnr, aac (6′)-Ib-cr and qepA genes in Escherichia coli isolated from cooked meat products in Henan, China. Int J Food Microbiol 187:22-5.
Kaper JB, Nataro JP, Mobley HL, 2004. Pathogenic escherichia coli. Nat Rev Microbiol 2:123-40.
Kaspar H, 2006. Results of the antimicrobial agent susceptibility study raised in a representative, cross-sectional monitoring study on a national basis. Int J Med Microbiol 41:69-79.
Kimura B, Kawasaki S, Fujii T, Kusunoki J, Itoh T, Flood SJA, 1999. Evaluation of TaqMan PCR Assay for Detecting Salmonella in Raw Meat and Shrimp. J Food Protect 62:329-35.
Lima CM, Souza IEGL, dos Santos Alves T, Leite CC, Evangelista-Barreto NS, de Castro Almeida RC, 2017. Antimicrobial resistance in diarrheagenic Escherichia coli from ready-to-eat foods. J Food Sci Tech 54:3612-9.
Liu CM, Stegger M, Aziz M, Johnson TJ, Waits K, Nordstrom L, Gauld L, Weaver B, Rolland D, Statham S, Horwinski J, Sariya S, Davis GS, Sokurenko E, Keim P, Johnson JR, Price LB, 2018. Escherichia coli ST131-H22 as a foodborne uropathogen. mBio 9:e00470-18.
MacDonald DM, Fyfe M, Paccagnella A, Trinidad A, Louie K, Patrick D, 2004. Escherichia coli O157:H7 outbreak linked to salami, British Columbia, Canada, 1999. Epidemiol Infect 132:283-9.
Mcauley CM, McMillan K, Moore SC, Fegan N, Fox EM, 2014. Prevalence and characterization of foodborne pathogens from Australian dairy farm environments. J Dairy Sci 97:7402-12.
Oliva M, Monno R, D’Addabbo P, Pesole G, Dionisi AM, Scrascia M, Chiara M, Horner DS, Manzari C, Luzzi I, Calia C, D’Erchia AM, Pazzani C, 2017. A novel group of IncQ1 plasmids conferring multidrug resistance. Plasmid 89:22-6.
Ombarak RA, Hinenoya A, Elbagory AM, Yamasaki S, 2018. Prevalence and molecular characterization of antimicrobial resistance in Escherichia coli isolated from raw milk and raw milk cheese in Egypt. J Food Prot 81:226-32.
Pakbin B, Brück WM, Rossen JWA, 2021. Virulence factors of enteric pathogenic Escherichia coli: a review. Int J Mol Sci 22:9922.
Pasquali F, Valero A, Possas A, Lucchi A, Crippa C, Gambi L, Manfreda G, De Cesare A, 2022. Occurrence of foodborne pathogens in Italian soft artisanal cheeses displaying different intra- and inter-batch variability of physicochemical and microbiological parameters. Front Microbiol 13:959648.
Pasquali F, Valero A, Possas A, Lucchi A, Crippa C, Gambi L, Manfreda G, De Cesare A, 2023. Variability in physicochemical parameters and its impact on microbiological quality and occurrence of foodborne pathogens in artisanal Italian organic salami. Foods 12:4086.
Ramos S, Silva V, Dapkevicius MLE, Caniça M, Tejedor-Junco MT, Igrejas G, Poeta P, 2020. Escherichia coli as commensal and pathogenic bacteria among food-producing animals: health implications of extended spectrum β-lactamase (ESBL) production. Animals 10:2239.
Rega M, Andriani L, Poeta A, Bonardi S, Conter M, Bacci C, 2023. The pork food chain as a route of transmission of antimicrobial resistant Escherichia coli: a farm-to-fork perspective. Antibiotics 12:376.
Rega M, Carmosino I, Bonilauri P, Frascolla V, Vismarra A, Bacci C, 2021. Prevalence of ESβL, AmpC and colistin-resistant E. coli in Meat: a comparison between pork and wild boar. Microorganisms 9:214.
Rehman MA, Rempel H, Carrillo CD, Ziebell K, Allen K, Manges AR, Topp E, Diarra MS, 2022. Virulence genotype and phenotype of multiple antimicrobial-resistant Escherichia coli isolates from broilers assessed from a “one-health” perspective. J Food Prot 85:336-54.
Reid CJ, Cummins ML, Börjesson S, Brouwer MSM, Hasman H, Hammerum AM, Roer L, Hess S, Berendonk T, Nešporová K, Haenni M, Madec JY, Bethe A, Michael GB, Schink AK, Schwarz S, Dolejska M, Djordjevic SP, 2022. A role for ColV plasmids in the evolution of pathogenic Escherichia coli ST58. Nat Commun 13:683.
Reid CJ, Wyrsch ER, Roy Chowdhury P, Zingali T, Liu M, Darling AE, Chapman TA, Djordjevic SP, 2017. Porcine commensal Escherichia coli: a reservoir for class 1 integrons associated with IS26. Microb Genom 3:e000143.
Sannes MR, Kuskowski MA, Owens K, Gajewski A, Johnson JR, 2004. Virulence factor profiles and phylogenetic background of Escherichia coli isolates from veterans with bacteremia and uninfected control subjects. J Infect Dis 190:2121-8.
Slinger R, Lau K, Slinger M, Moldovan I, Chan F, 2017. Higher atypical enteropathogenic Escherichia coli (a-EPEC) bacterial loads in children with diarrhea are associated with PCR detection of the EHEC factor for adherence 1/lymphocyte inhibitory factor A (efa1/lifa) gene. Ann Clin Microbiol Antimicrob 16:16.
Trmčić A, Chauhan K, Kent DJ, Ralyea RD, Martin NH, Boor KJ, Wiedmann M, 2016. Coliform detection in cheese is associated with specific cheese characteristics, but no association was found with pathogen detection. J Dairy Sci, 99:6105-20.
Wyrsch ER, Bushell RN, Marenda MS, Browning GF, Djordjevic SP, 2022. Global phylogeny and F virulence plasmid carriage in pandemic Escherichia coli ST1193. Microbiol Spectr 10:e02554-22.
Xu Y, Bai X, Jin Y, Hu B, Wang H, Sun H, Fan R, Fu S, Xiong Y, 2017. High Prevalence of Virulence Genes in Specific Genotypes of Atypical Enteropathogenic Escherichia coli. Front Cell Infect Microbiol 7:109.
Yang S, Pei X, Wang G, Yan L, Hu J, Li Y, Li N, Yang D, 2016. Prevalence of food-borne pathogens in ready-to-eat meat products in seven different Chinese regions. Food Control 65:92-8.
Yang SC, Lin CH, Aljuffali IA, Fang JY, 2017. Current pathogenic Escherichia coli foodborne outbreak cases and therapy development. Arch Microbiol 199:811-25.

How to Cite

1.
Crippa C, De Cesare A, Lucchi A, Parisi A, Manfreda G, Pasquali F. Occurrence and genomic characterization of antimicrobial-resistant and potential pathogenic <i>Escherichia coli</i> from Italian artisanal food productions of animal origin. Ital J Food Safety [Internet]. 2024 Mar. 25 [cited 2024 Jul. 13];13(2). Available from: https://www.pagepressjournals.org/ijfs/article/view/12205