https://doi.org/10.4081/ijfs.2022.10899
Resistome and virulome diversity of foodborne pathogens isolated from artisanal food production chain of animal origin in the Mediterranean region
Published: 5 December 2022
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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.
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The aim of the present study was to investigate the resistome and virulome diversity of 43 isolates of Listeria monocytogenes, Salmonella enterica and S. aureus collected from artisanal fermented meat and dairy products and their production environments in Portugal, Spain, Italy and Morocco. After DNA extraction, genomes were sequenced, and de novo assembled. Genetic relationships among genomes were investigated by SNP calling and in silico 7- loci MLST. Genomes of the same species belonged to different ST-types demonstrating the circulation of different clones in in the same artisanal production plant. One specific clone included genomes of S. Paratyphi B belonging to ST43 and repeatedly isolated for more than a year in an artisanal sausage production plant. No genomes but three (belonging to Salmonella enterica), were predicted as multiresistant to different antimicrobials classes. Regarding virulence, genomes of L. monocytogenes belonging to ST1, ST3 and ST489, as well as genomes of S.enterica enterica (ST43, ST33, ST314, ST3667, ST1818, ST198) and ST121 S. aureus were predicted as virulent and hypervirulent. The occurrence of virulent and hypervirulent L. monocytogenes, Salmonella enterica and S. aureus strains in artisanal fermented meat and dairy productions as well as in their finished products suggests the need for a specific focus on prevention and control measures able to reduce the risk of these biological hazards in artisanal food productions.
Abebe E, Gugsa G, Ahmed M, 2020. Review on major food-borne zoonotic bacterial pathogens. J Trop Med 2020:4674235.
DOI: https://doi.org/10.1155/2020/4674235
Alsayeqh AF, Baz AHA, Darwish WS, 2021. Antimicrobial-resistant foodborne pathogens in the Middle East: A systematic review. Environ Sci Pollut Res 28:68111-33.
DOI: https://doi.org/10.1007/s11356-021-17070-9
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.
DOI: https://doi.org/10.1016/j.cmi.2017.10.013
Castellanos LR, van der Graaf-van Bloois L, Donado-Godoy P, Veldman K, Duarte F, Acuña MT, Jarquín C, Weill FX, Mevius DJ, Wagenaar JA, Hordijk J, Zomer AL, 2020. Antimicrobial resistance in Salmonella enterica serovar paratyphi B variant Java in poultry from Europe and Latin America. Emerg Infect Dis 26:1164-73.
DOI: https://doi.org/10.3201/eid2606.191121
Capozzi V, Fragasso M, Russo P, 2020. Microbiological safety and the management of microbial resources in artisanal foods and beverages: The need for a transdisciplinary assessment to conciliate actual trends and risks avoidance. Microorganisms 8:306.
DOI: https://doi.org/10.3390/microorganisms8020306
Carroll LM, Pierneef R, Mathole M, Matle I, 2021. Genomic characterization of endemic and ecdemic non-typhoidal Salmonella enterica lineages circulating among animals and animal products in South Africa. Front Microbiol 12:748611.
DOI: https://doi.org/10.3389/fmicb.2021.748611
Deurenberg RH, Vink C, Kalenic S, Friedrich AW, Bruggeman CA, Stobberingh EE, 2007. The molecular evolution of methicillin-resistant Staphylococcus aureus. Clin Miocrobiol Infect 13:222-35.
DOI: https://doi.org/10.1111/j.1469-0691.2006.01573.x
Ditlevsen, K, Denver S, Christensen T, Lassen J, 2020. A taste for locally produced food-Values, opinions and sociodemographic differences among ‘organic’ and ‘conventional’ consumers. Appetite 147:104544.
DOI: https://doi.org/10.1016/j.appet.2019.104544
EFSA and ECDC (European Food Safety Authority and European Centre for Disease Prevention and Control), 2021a. The European Union One Health 2020 Zoonoses Report. EFSA Journal 19:6971 324 pp.
DOI: https://doi.org/10.2903/j.efsa.2021.6971
EFSA and ECDC (European Food Safety Authority and European Centre for Disease Prevention and Control), 2021b. The European Union Summary Report on Antimicrobial Resistance in zoonotic and indicator bacteria from humans, animals and food in 2018/2019. EFSA Journal 19:6490, 179 pp.
DOI: https://doi.org/10.2903/j.efsa.2021.6490
Frizzo F, Dias HBA, Duarte NP, Rodrigues DG, Prado PHM, 2020. The genuine handmade: How the production method influences consumers’ behavioral intentions through naturalness and authenticity. J Food Prod Mark 26:279-96.
DOI: https://doi.org/10.1080/10454446.2020.1765936
Ghebremedhin B, Olugbosi MO, Raji AM, Layer F, Bakare RA, Konig B, Konig W, 2009. Emergence of a community-associated methicillin-resistant Staphylococcus aureus strain with a unique resistance profile in Southwest Nigeria. J Clin Microbiol 47:2975-80.
DOI: https://doi.org/10.1128/JCM.00648-09
Gourama H, 2020. Foodborne pathogens. In: Demirici A, Feng H, Krishnamurthy K (eds). Food Safety Engineering. Food Engineering Series. Spinger, Cham pp. 25-49.
DOI: https://doi.org/10.1007/978-3-030-42660-6_2
Graham JP, Eisenberg JN, Trueba G, Zhang L, Johnson TJ, 2017. Small-scale food animal production and antimicrobial resistance: mountain, molehill, or something in-between?. Environ Health Perspect 125:104501.
DOI: https://doi.org/10.1289/EHP2116
Halagarda M, Wójciak KM, 2022. Health and safety aspects of traditional European meat products. A review. Meat Sci 184:108623.
DOI: https://doi.org/10.1016/j.meatsci.2021.108623
Heaton CJ, Gerbig GR, Sensius LD, Patel V, Smith TC 2020. Staphylococcus aureus epidemiology in wildlife: A systematic review. Antibiotics 9:89.
DOI: https://doi.org/10.3390/antibiotics9020089
Hiramatsu K, Ito T, Tsubakishita S, Sasaki T, Takeuchi F, Morimoto Y, Katayama Y, Matsuo M, Kuwahara-Arai K, Hishinuma T, Baba T. Genomic Basis for Methicillin Resistance in Staphylococcus aureus. Infect Chemother 45:117-36.
DOI: https://doi.org/10.3947/ic.2013.45.2.117
Ho TD, Slauch JM, 2001. Characterization of grvA, an antivirulence gene on the gifsy-2 phage in Salmonella enterica serovar typhimurium. J Bacteriol 183:611-20.
DOI: https://doi.org/10.1128/JB.183.2.611-620.2001
Hu Q, Cheng H, Yuan W, Zeng F, Shang W, Tang D, Xue W, Fu J, Zhou R, Zhu J, Yang J, Hu Z, Yuan J, Zhang X, Rao Q, Li S, Chen Z, Hu X, Wu X, Rao X. Panton-Valentine leukocidin (PVL)-positive health care-associated methicillin-resistant Staphylococcus aureus isolates are associated with skin and soft tissue infections and colonized mainly by infective PVL-encoding bacteriophages. J Clin Microbiol 53:67-72.
DOI: https://doi.org/10.1128/JCM.01722-14
Letunic I, Bork P, 2021. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 49:293-96.
DOI: https://doi.org/10.1093/nar/gkab301
Lv G, Jiang R, Zhang H, Wang L, Li L, Gao W, Zhang H, Pei Y, Wei X, Dong H, Qin L. Molecular Characteristics of Staphylococcus aureus From Food Samples and Food Poisoning Outbreaks in Shijiazhuang, China. Front Microbiol 12:652276.
DOI: https://doi.org/10.3389/fmicb.2021.652276
Marcus SL, Brumell JH, Pfeifer CG, Finlay BB. Salmonella pathogenicity islands: big virulence in small packages. Microbes Infect 2:145-56.
DOI: https://doi.org/10.1016/S1286-4579(00)00273-2
Palma F, Manfreda G, Silva M, Parisi A, Barker DO, Taboada EN, Pasquali F, Rossi M, 2018. Genome-wide identification of geographical segregated genetic markers in Salmonella enterica serovar Typhimurium variant 4,[5], 12: i:-. Scientific Reports 8:1-12.
DOI: https://doi.org/10.1038/s41598-018-33266-5
Pasquali F, Valero A, Possas A, Lucchi A, Crippa C, Gambi L, Manfreda G and
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
Rao SN, Rhodes NJ, Lee BJ, Scheetz MH, Hanson AP, Segreti J., Crank CW, Wang, S. K. (2015). Treatment outcomes with cefazolin versus oxacillin for deep-seated methicillin-susceptible Staphylococcus aureus bloodstream infections. Antimicrob Agents Chemother 59:5232-38.
DOI: https://doi.org/10.1128/AAC.04677-14
Tamang JP, Cotter PD, Endo A, Han NS, Kort R, Liu SQ, Mayo B, Westerik N, Hutkins R. Fermented foods in a global age: East meets West. Compr Rev Food Sci Food Saf 19:184-217.
DOI: https://doi.org/10.1111/1541-4337.12520
van Belkum A, Melles DC, Peeters JK, van Leeuwen WB, van Duijkeren E, Huijsdens XW, Spalburg E, de Neeling AJ, Verbrugh HA; Dutch Working Party on Surveillance and Research of MRSA-SOM. Methicillin-resistant and -susceptible Staphylococcus aureus sequence type 398 in pigs and humans. Emerg Infect Dis. 2008 Mar;14:479-83.
DOI: https://doi.org/10.3201/eid1403.070760
Vilchis-Rangel RE, Espinoza-Mellado M, del R Salinas-Jaramillo IJ, Martinez-Peña MD, Rodas-Suárez OR, 2019. Association of Listeria Monocytogenes LIPI-1 and LIPI-3 Marker llsX With Invasiveness. Curr Microbiol 6:637-643.
DOI: https://doi.org/10.1007/s00284-019-01671-2
Word Health Organizazion (WHO), 2021. Antimicrobial resistance. https://www.who.int/news-room/fact-sheets/detail/antimicrobial-resistance Accessed: August 29th, 2022.
Supporting Agencies
This work was funded within the EU H2020 PRIMA Project ArtiSaneFood “Innovative bio-interventions and risk modelling approaches for ensuring microbial safety and quality of Mediterranean artisanal fermented foods” (PRIMA/0001/2018). U. Gonzales-Barron and V. Cadavez are also grateful to the Portuguese Foundation for Science and Technology (FCT) for funding PRIMA/0001/2018; and for financial support through national funds FCT/MCTES (PIDDAC) to CIMO (UIDB/00690/2020 and UIDP/00690/2020) and SusTEC (LA/P/0007/2021).How to Cite
1.
Pasquali F, Gambi L, De Cesare A, Crippa C, Cadavez V, Gonzales-Barron U, Valero A, Achemchem F, Lucchi A, Parisi A, Manfreda G. Resistome and virulome diversity of foodborne pathogens isolated from artisanal food production chain of animal origin in the Mediterranean region. Ital J Food Safety [Internet]. 2022 Dec. 5 [cited 2024 Nov. 28];11(4). Available from: https://www.pagepressjournals.org/ijfs/article/view/10899
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