Raw milk cheeses from Beira Baixa, Portugal-A contributive study for the microbiological hygiene and safety assessment.

Escherichia coli Listeria monocytogenes Salmonella spp. Coagulase Positive Staphylococci Portugal Raw milk cheese Whole-genome sequencing (WGS)

Journal

Brazilian journal of microbiology : [publication of the Brazilian Society for Microbiology]
ISSN: 1678-4405
Titre abrégé: Braz J Microbiol
Pays: Brazil
ID NLM: 101095924

Informations de publication

Date de publication:
15 Apr 2024
Historique:
received: 21 12 2023
accepted: 03 04 2024
medline: 16 4 2024
pubmed: 16 4 2024
entrez: 15 4 2024
Statut: aheadofprint

Résumé

Due to specific bacterial microbiota, raw milk cheeses have appreciated sensory properties. However, they may pose a threat to consumer safety due to potential pathogens presence. This study evaluated the microbiological contamination of 98 raw milk cheeses from Beira Baixa, Portugal. Presence and enumeration of Coagulase Positive Staphylococci (CPS), Listeria monocytogenes, Salmonella spp., pathogenic Escherichia coli, and indicator microorganisms (non-pathogenic E. coli and Listeria spp.) was attained. E. coli antimicrobial resistance (AMR) was also evaluated. PCR and/or Whole genome sequencing (WGS) was used to characterize E. coli, Salmonella spp. and L. monocytogenes isolates. Sixteen cheeses (16.3%) were classified as Satisfactory, 59 (60.2%) as Borderline and 23 (23.5%) as Unsatisfactory/Potential Injurious to Health. L. monocytogenes, CPS > 10

Identifiants

pubmed: 38622468
doi: 10.1007/s42770-024-01332-y
pii: 10.1007/s42770-024-01332-y
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s).

Références

Casalta E, Sorba JM, Aigle M, Ogier JC (2009) Diversity and dynamics of the microbial community during the manufacture of Calenzana, an artisanal Corsican cheese. Int J Food Microb 133:243–251. https://doi.org/10.1016/j.ijfoodmicro.2009.05.022
doi: 10.1016/j.ijfoodmicro.2009.05.022
Chambers D, Esteve E, Retiveau AR (2010) Effect of milk pasteurization on flavor properties of seven commercially available French cheese types. J Sens Stud 25:494–511. https://doi.org/10.1111/j.1745-459X.2010.00282.x
doi: 10.1111/j.1745-459X.2010.00282.x
Masoud W, Vogensen FK, Lillevang S, Abu Al-Soud W, Sørensen SJ, Jakobsen M (2012) The fate of indigenous microbiota, starter cultures, Escherichia coli, Listeria innocua and Staphylococcus aureus in Danish raw milk and cheeses determined by pyrosequencing and quantitative real time (qRT)- PCR. Int J Food Microbiol 153(1–2):192–202. https://doi.org/10.1016/j.ijfoodmicro.2011.11.014
doi: 10.1016/j.ijfoodmicro.2011.11.014 pubmed: 22154239
Debarry J, Garn H, Hanuszkiewicz A, Dickgreber N, Blumer N, von Mutius E, Bufe A, Gatermann S, Renz H, Holst O, Heine H (2007) Acinetobacter lwoffii and Lactococcus lactis strains isolated from farm cowsheds possess strong allergy-protective properties. J Allergy Clin Immunol 119:1514–1521. https://doi.org/10.1016/j.jaci.2007.03.023
doi: 10.1016/j.jaci.2007.03.023 pubmed: 17481709
Ege MJ, Mayer M, Schwaiger K, Mattes J, Pershagen G, van Hage M, Scheynius A, Bauer J, von Mutius E (2012) Environmental bacteria and childhood asthma. Allergy 67(12):1565–1571. https://doi.org/10.1111/all.12028
doi: 10.1111/all.12028 pubmed: 22994424
Crippa G, Zabzuni D, Bravi E, Piva G, De Noni I, Bighi E, Rossi F (2018) Randomized, Double Blind Placebo-Controlled Pilot Study of the Antihypertensive Effects of Grana Padano D.O.P. Cheese Consumption in Mild—Moderate Hypertensive Subjects. Eur Rev Med Pharmacol Sci 22:7573–7581. https://doi.org/10.26355/eurrev_201811_16299
Oliver SP, Jayarao BM, Almeida RA (2005) Foodborne pathogens in milk and the dairy farm environment: food safety and public health implications. Foodborne Pathog Dis 2(2):115–129. https://doi.org/10.1089/fpd.2005.2.115
doi: 10.1089/fpd.2005.2.115 pubmed: 15992306
Langer AJ, Ayers T, Grass J, Lynch M, Angulo FJ, Mahon BE (2012) Nonpasteurized dairy products, disease outbreaks, and state laws—United States, 1993–2006. Emerg Infect Dis 18(3):385–391. https://doi.org/10.3201/eid1803.111370
doi: 10.3201/eid1803.111370 pubmed: 22377202 pmcid: 3309640
Costard S, Espejo L, Groenendaal H, Zagmutt FJ (2017) Outbreak-related disease burden associated with consumption of unpasteurized cow’s milk and cheese, United States, 2009–2014. Emerg Infect Dis 23:957–964. https://doi.org/10.3201/eid2306.151603
doi: 10.3201/eid2306.151603 pubmed: 28518026 pmcid: 5443421
Possas A, Bonilla-Luque OM, Valero A (2021) From Cheese-Making to Consumption: Exploring the Microbial Safety of Cheeses through Predictive Microbiology Models. Foods 10(2):355. https://doi.org/10.3390/foods10020355
doi: 10.3390/foods10020355 pubmed: 33562291 pmcid: 7915996
André MCDPB, Campos MRH, Borges LJ, Kipnis A, Pimenta FC, Serafini ÁB (2008) Comparison of Staphylococcus aureus isolates from food handlers, raw bovine milk and Minas Frescal cheese by antibiogram and pulsed-field gel electrophoresis following SmaI digestion. Food Control 19:200–207. https://doi.org/10.1016/j.foodcont.2007.03.010
doi: 10.1016/j.foodcont.2007.03.010
Schön K, Schornsteiner E, Dzieciol M, Wagner M, Müller M, Schmitz-Esser S (2016) Microbial communities in dairy processing environment floor-drains are dominated by product-associated bacteria and yeasts. Food Control 70:210–215. https://doi.org/10.1016/j.foodcont.2016.05.057
doi: 10.1016/j.foodcont.2016.05.057
Kousta M, Mataragas M, Skandamis P, Drosinos EH (2010) Prevalence and sources of cheese contamination with pathogens at farm and processing levels. Food Control 21(6):805–815. https://doi.org/10.1016/j.foodcont.2009.11.015
doi: 10.1016/j.foodcont.2009.11.015
Official European Union website, EFSA Foodborne outbreaks – dashboard. https://www.efsa.europa.eu/en/microstrategy/FBO-dashboard . Accessed 27 March 20234
Dias J (2022) The use of cheese from Alentejo in Portuguese gastronomy: A travel through history. Int J Gastron Food Sci 29:100579. https://doi.org/10.1016/j.ijgfs.2022.100579
doi: 10.1016/j.ijgfs.2022.100579
European Commission. Agriculture and rural development. Geographical indications and quality schemes explained. https://agriculture.ec.europa.eu/farming/geographical-indications-and-quality-schemes/geographical-indications-and-quality-schemes-explained_en . Accessed 27 March 2024
ISO 7218:2007, Microbiology of food and animal feeding stuffs — General requirements and guidance for microbiological examinations.
ISO 6579–1:2017 Microbiology of the food chain- Horizontal method for the detection, enumeration and serotyping of Salmonella
ISO 11290–1:2017, Microbiology of food chain — Horizontal methos for the detection and enumeration of Listeria monocytogenes and of Listeria spp. — Part 1: Detection method
ISO 11290–2:2017, Microbiology of food chain — Horizontal methos for the detection and enumeration of Listeria monocytogenes and of Listeria spp. — Part 2: Enumeration method
ISO 19020:2017, Microbiology of food chain — Horizontal methos for the immunoenzymatic detection of staphylococcal enterotoxins in foodstuffs
Instituto Nacional de Saúde Doutor Ricardo Jorge. Interpretação de resultados de ensaios microbiológicos em alimentos prontos para consumo e em superfícies do ambiente de preparação e distribuição alimentar: valores-guia. Lisboa: INSA IP, 2019. http://repositorio.insa.pt/bitstream/10400.18/5610/3/INSA_Interpreta%c3%a7%c3%a3o%20de%20resultados%20de%20ensaios%20microbiol%c3%b3gicos_Valores-guia_2019.pdf . Accessed 27 March 2024.
Commission Regulation (EC) Nº 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. Official Journal of the European Union: L338/1-L338/26. https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32005R2073 . Accessed 27 March 2024.
HPA. (2009). Guidelines for Assessing the Microbiological Safety of Ready-to-Eat Foods Placed on the Market. Health Protection Agency, London. https://assets.publishing.service.gov.uk/media/5a7efde0e5274a2e8ab497a4/Guidelines_for_assessing_the_microbiological_safety_of_ready-to-eat_foods_on_the_market.pdf . Accessed 27 March 2024.
Luxembourg Ministère de la Santé, Critères microbiologiques applicables aux denrées alimentaires- Lignes directrices pour l’interprétation. F-054 Rev05; 2018. https://securite-alimentaire.public.lu/dam-assets/fr/professionnel/Denrees-alimentaires/Qualite-microbiologique/recueil_criteres_microbiologiques/F-054-05.pdf .Accessed 27 March 2024.
EUCAST The European Committee on Antimicrobial Susceptibility Testing. Breakpoint Tables for Interpretation of MICs and Zone Diameters. http://www.eucast.org . Accessed 27 March 2024.
Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B et al (2011) Multidrugresistant, extensively drugresistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 18(3):268–281. https://doi.org/10.1111/j.1469-0691.2011.03570.x
doi: 10.1111/j.1469-0691.2011.03570.x pubmed: 21793988
Grimont PAD, Weill FX (2007) Antigenic formulae of the Salmonella serovars. In: WHO collaborating centre for reference and research on Salmonella, 9th edn. WHO Collaborating Centre for reference and research on Salmonella: Institute Pasteur, France, pp. 1–166.
Pista A, Silveira L, Ribeiro S, Fontes M, Castro R, Coelho A, Furtado R, Lopes T, Maia C, Mixão V, et. al. (2022) Pathogenic Escherichia coli, Salmonella spp. and Campylobacter spp. in Two Natural Conservation Centers of Wildlife in Portugal: Genotypic and Phenotypic Characterization. Microorganisms 10(11):2132. doi: https://doi.org/10.3390/microorganisms10112132
Sora VM, Meroni G, Martino PA, Soggiu A, Bonizzi L, Zecconi A (2021) Extraintestinal Pathogenic Escherichia coli: Virulence Factors and Antibiotic Resistance. Pathogens 10(11):1355. https://doi.org/10.3390/pathogens10111355
doi: 10.3390/pathogens10111355 pubmed: 34832511 pmcid: 8618662
Llarena A-K, Ribeiro-Gonçalves BF, Silva DN, Halkilahti J, Machado MP, Da Silva MS, Jaakkonen A, Isidro J, Hämäläinen C, Joenperä J et al (2018) INNUENDO: A Cross-sectoral Platform for the Integration of Genomics in the Surveillance of Food-borne Pathogens. EFSA Support Publ 15:1498E. https://doi.org/10.2903/sp.efsa.2018.EN-1498
doi: 10.2903/sp.efsa.2018.EN-1498
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
doi: 10.1093/bioinformatics/btu170 pubmed: 24695404 pmcid: 4103590
Prjibelski A, Antipov D, Meleshko D, Lapidus A, Korobeynikov A (2020) Using SPAdes De Novo Assembler. Curr Protoc Bioinform 70(1):e102. https://doi.org/10.1002/cpbi.102
doi: 10.1002/cpbi.102
Langmead B (2010) Aligning Short Sequencing Reads with Bowtie. Curr Protoc Bioinform 32:11.7.1–11.7.14. https://doi.org/10.1002/0471250953.bi1107s32
Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, Cuomo CA, Zeng Q, Wortman J, Young SK et al (2014) Pilon: An Integrated Tool for Comprehensive Microbial Variant Detection and Genome Assembly Improvement. PLoS ONE 9(11):e112963. https://doi.org/10.1371/journal.pone.0112963
doi: 10.1371/journal.pone.0112963 pubmed: 25409509 pmcid: 4237348
Wood DE, Salzberg SL (2014) Kraken: Ultrafast Metagenomic Sequence Classification Using Exact Alignments. Genome Biol 15(3):R46. https://doi.org/10.1186/gb-2014-15-3-r46
doi: 10.1186/gb-2014-15-3-r46 pubmed: 24580807 pmcid: 4053813
Silva M, Machado MP, Silva DN, Rossi M, Moran-Gilad J, Santos S, Ramirez M, Carriço JA (2018) chewBBACA: A Complete Suite for Gene-by-Gene Schema Creation and Strain Identification. Microb Genom 4(3):e000166. https://doi.org/10.1099/mgen.0.000166
doi: 10.1099/mgen.0.000166 pubmed: 29543149 pmcid: 5885018
Moura A, Criscuolo A, Pouseele H, Maury MM, Leclercq A, Tarr C, Björkman JT, Dallman T, Reimer A, Enouf V et al (2016) Whole genome-based population biology and epidemiological surveillance of Listeria monocytogenes. Nat Microbiol 2:16185. https://doi.org/10.1038/nmicrobiol.2016.185
doi: 10.1038/nmicrobiol.2016.185 pubmed: 27723724 pmcid: 8903085
Mamede R, Vila-Cerqueira P, Silva M, Carriço JA, Ramirez M (2020) Chewie Nomenclature Server (chewie-NS): A Deployable Nomenclature Server for Easy Sharing of Core and Whole Genome MLST Schemas. Nucleic Acids Res 49:D660–D666. https://doi.org/10.1093/nar/gkaa889
doi: 10.1093/nar/gkaa889 pmcid: 7778912
Mixão V, Pinto M, Sobral D, Di Pasquale A, Gomes JP, Borges V (2023) ReporTree: a surveillance-oriented tool to strengthen the linkage between pathogen genetic clusters and epidemiological data. Genome Med 15(1):43. https://doi.org/10.1186/s13073-023-01196-1
doi: 10.1186/s13073-023-01196-1 pubmed: 37322495 pmcid: 10273728
Zhou Z, Alikhan N-F, Sergeant MJ, Luhmann N, Vaz C, Francisco AP, Carriço JA, Achtman M (2018) GrapeTree: Visualization of Core Genomic Relationships among 100,000 Bacterial Pathogens. Genome Res 28(9):1395–1404. https://doi.org/10.1101/gr.232397.117
doi: 10.1101/gr.232397.117 pubmed: 30049790 pmcid: 6120633
VanWalle I, Björkman JT, Cormican M, Dallman T, Mossong J, Moura A, Pietzka A, Ruppitsch W, Takkinen J (2018) European Listeria WGS typing group. Retrospective validation of whole genome sequencing-enhanced surveillance of listeriosis in Europe, 2010 to 2015. Eurosurveillance 23(33):1700798. https://doi.org/10.2807/1560-7917.ES.2018.23.33.1700798
Treangen TJ, Ondov BD, Koren S, Phillippy AM (2014) The Harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol 15(11):524. https://doi.org/10.1186/s13059-014-0524-x
doi: 10.1186/s13059-014-0524-x pubmed: 25410596 pmcid: 4262987
Kim K, Lee H, Gwak E, Yon Y (2014) Kinetic behavior of Escherichia coli on various cheeses under constant and dynamic temperature. Asian-Australas J Anim Sci 27(7):1013–1018. https://doi.org/10.5713/ajas.2013.13579
doi: 10.5713/ajas.2013.13579 pubmed: 25050044 pmcid: 4093577
Lahou E, Uyttendaele M (2017) Growth potential of Listeria monocytogenes in soft, semi-soft and semi-hard artisanal cheeses after post-processing contamination in deli retail establishments. Food Control 76:13–23. https://doi.org/10.1016/j.foodcont.2016.12.033
doi: 10.1016/j.foodcont.2016.12.033
Gonzales-Barro U, Gonçalves-Tenório A, Rodrigues A, Cadavez V (2017) Foodborne pathogens in raw milk and cheese of sheep and goat origin: a meta-analysis approach. Curr Opin Food Sci 18:7–13. https://doi.org/10.1016/j.cofs.2017.10.002
doi: 10.1016/j.cofs.2017.10.002
Magalhães R, Almeida G, Ferreira V, Santos I, Silva J, Mendes MM, Pita J, Mariano G, Mâncio I, Sousa MM et al (2015) Cheese-related listeriosis outbreak, Portugal, March 2009 to February 2012. Eurosurveill J 20(17):21104. https://doi.org/10.2807/1560-7917.es2015.20.17.21104
doi: 10.2807/1560-7917.es2015.20.17.21104
de Castro V, Escudero JM, Rodriguez JL, Muniozguren N, Uribarri J, Saez D, Vazquez J (2012) Listeriosis outbreak caused by Latin-style fresh cheese, Bizkaia, Spain, August 2012. Eurosurveillance 17(42):20298
doi: 10.2807/ese.17.42.20298-en pubmed: 23098823
Amato E, Filipello V, Gori M, Lomonaco S, Losio MN, Parisi A, Huedo P, Knabel SJ, Pontello M (2017) Identification of a major Listeria monocytogenes outbreak clone linked to soft cheese in Northern Italy—2009–2011. BMC Infect Dis 17:1–7. https://doi.org/10.1186/s12879-017-2441-6
doi: 10.1186/s12879-017-2441-6
Fretz R, Pichler J, Sagel U, Much P, Ruppitsch W, Pietzka AT, Stöger A, Huhulescu S, Heuberger S, Appl G et al (2010) Update: Multinational listeriosis outbreak due to “quargel”, a sour milk curd cheese, caused by two different L. monocytogenes serotype 1/2a strains, 2009–2010. Eurosurveillance 15(16):19543
Koch J, Dworak R, Prager R, Becker B, Brockmann S, Wicke A, Wichmann- Schauer H, Hof H, Werber D, Stark K (2010) Large listeriosis outbreak linked to cheese made from pasteurized milk, Germany, 2006–2007. Foodborne Pathog Dis 7(12):1581–1584. https://doi.org/10.1089/fpd.2010.0631
doi: 10.1089/fpd.2010.0631 pubmed: 20807110
The European Parliament and the Council of the European Union. Regulation (EC) No 852/2004 of the European Parliament and of the Council of 29 April 2004 on the hygiene of foodstuffs (2004). Official Journal of the European Communities L139/1
Painset A, Björkman JT, Kiil K, Guillier L, Mariet JF, Félix B, Amar C, Rotariu O, Roussel S, Perez-Reche F et al (2019) LiSEQ—Whole-genome sequencing of a cross-sectional survey of Listeria monocytogenes in ready-to-eat foods and human clinical cases in Europe. Microb Genom 5(2):e000257. https://doi.org/10.1099/mgen.0.000257
doi: 10.1099/mgen.0.000257 pubmed: 30775964 pmcid: 6421348
Vallejo P, Cilla G, López-Olaizola M, Vicente D, Marimón JM (2022) Epidemiology and Clinical Features of Listeriosis in Gipuzkoa, Spain, 2010–2020. Front Microbiol 13:894334. https://doi.org/10.3389/fmicb.2022.894334
doi: 10.3389/fmicb.2022.894334 pubmed: 35755994 pmcid: 9218358
Muhterem-Uyar M, Ciolacu L, Wagner KH, Wagner M, Schmitz-Esser S, Stessl B (2018) New Aspects on Listeria monocytogenes ST5-ECVI Predominance in a Heavily Contaminated Cheese Processing Environment. Front Microbiol 9:64. https://doi.org/10.3389/fmicb.2018.00064
doi: 10.3389/fmicb.2018.00064 pubmed: 29472901 pmcid: 5810274
Andritsos ND, Mataragas M (2023) Characterization and Antibiotic Resistance of Listeria monocytogenes Strains Isolated from Greek Myzithra Soft Whey Cheese and Related Food Processing Surfaces over Two-and-a-Half Years of Safety Monitoring in a Cheese Processing Facility. Foods 12(6):1200. https://doi.org/10.3390/foods12061200
doi: 10.3390/foods12061200 pubmed: 36981126 pmcid: 10048787
Kaszoni-Rückerl I, Mustedanagic A, Muri-Klinger S, Brugger K, Wagner KH, Wagner M, Stessl B (2020) Predominance of Distinct Listeria innocua and Listeria monocytogenes in Recurrent Contamination Events at Dairy Processing Facilities. Microorganisms 8(2):234. https://doi.org/10.3390/microorganisms8020234
doi: 10.3390/microorganisms8020234 pubmed: 32050536 pmcid: 7074772
Castro RD, Pedroso SHSP, Sandes SHC, Silva GO, Luiz KCM, Dias RS, Filho RAT, Figueiredo HCP, Santos SG, Nunes AC et al (2020) Virulence factors and antimicrobial resistance of Staphylococcus aureus isolated from the production process of Minas artisanal cheese from the region of Campo das Vertentes, Brazil. J Dairy Sci 103:2098–2110. https://doi.org/10.3168/jds.2019-17138
doi: 10.3168/jds.2019-17138 pubmed: 31980224
Fusco V, Chieffi D, Fanelli F, Logrieco AF, Cho GS, Kabisch J, Böhnlein C, Franz CMAP (2020) Microbial quality and safety of milk and milk products in the 21st century. Compr Rev Food Sci Food Saf 19:2013–2049. https://doi.org/10.1111/1541-4337.12568
doi: 10.1111/1541-4337.12568 pubmed: 33337106
Qi Y, Miller KJ (2000) Effect of low water activity on staphylococcal enterotoxin A and B biosynthesis. J Food Prot 63(4):473–478. https://doi.org/10.4315/0362-028x-63.4.473
doi: 10.4315/0362-028x-63.4.473 pubmed: 10772212
De Buyser ML, Dufour B, Maire M, Lafarge V (2001) Implication of milk and milk products in food-borne diseases in France and in different industrialised countries. Int J Food Microbiol 67(1–2):1–17. https://doi.org/10.1016/s0168-1605(01)00443-3
doi: 10.1016/s0168-1605(01)00443-3 pubmed: 11482557
Pineda APA, Campos GZ, Pimentel-Filho NJ, Franco BDGM, Pinto UM (2021) Brazilian Artisanal Cheeses: Diversity, Microbiological Safety, and Challenges for the Sector. Front Microbiol 12:666922. https://doi.org/10.3389/fmicb.2021.666922
doi: 10.3389/fmicb.2021.666922 pubmed: 33959118 pmcid: 8093504
Robinson E, Travanut M, Fabre L, Larréché S, Ramelli L, Pascal L, Guinard A, Vincent N, Calba C, Meurice L et al (2020) Outbreak of Salmonella Newport associated with internationally distributed raw goats’ milk cheese, France, 2018. Epidemiol Infect 148:e180. https://doi.org/10.1017/S0950268820000904
doi: 10.1017/S0950268820000904 pubmed: 32364094 pmcid: 7482037
Plumb ID, Schwensohn CA, Gieraltowski L, Tecle S, Schneider ZD, Freiman J, Cote A, Noveroske D, Kolsin J, Brandenburg J et. al. (2019) Outbreak of Salmonella Newport Infections with Decreased Susceptibility to Azithromycin Linked to Beef Obtained in the United States and Soft Cheese Obtained in Mexico—United States, 2018–2019. Morb Mortal Wkly Rep 68(33):713–717. https://doi.org/10.15585/mmwr.mm6833a1
Vignaud ML, Cherchame E, Marault M, Chaing E, Le Hello S, Michel V, Jourdan-Da Silva N, Lailler R, Brisabois A, Cadel-Six S (2017) MLVA for Salmonella enterica subsp. enterica serovar Dublin: Development of a method suitable for inter-laboratory surveillance and application in the context of a raw milk cheese outbreak in France in 2012. Front Microbiol 8:295. https://doi.org/10.3389/fmicb.2017.00295 .
Ung A, Baidjoe AY, Van Cauteren D, Fawal N, Fabre L, Guerrisi C, Danis K, Morand A, Donguy MP, Lucas E et al (2019) Disentangling a complex nationwide Salmonella Dublin outbreak associated with raw-milk cheese consumption, France, 2015 to 2016. Eurosurveillance 24(3):1700703. https://doi.org/10.2807/1560-7917.ES.2019.24.3.1700703
doi: 10.2807/1560-7917.ES.2019.24.3.1700703 pubmed: 30670140 pmcid: 6344836
Jones G, Lefèvre S, Donguy MP, Nisavanh A, Terpant G, Fougère E, Vaissière E, Guinard A, Mailles A, de Valk H et al (2019) Soutbreak of shiga toxin-producing Escherichia coli (STEC) O26 paediatric haemolytic uraemic syndrome (HUS) cases associated with the consumption of soft raw cow’s milk cheeses, France, march to May 2019. Eurosurveillance 24(22):1900305. https://doi.org/10.2807/1560-7917.ES.2019.24.22.1900305
doi: 10.2807/1560-7917.ES.2019.24.22.1900305 pubmed: 31164190 pmcid: 6549459
Currie A, Galanis E, Chacon PA, Murray R, Wilcott L, Kirkby P, Honish L, Franklin K, Farber J, Parker R et al (2013) (2018) Outbreak of Escherichia coli O157:H7 Infections Linked to Aged Raw Milk Gouda Cheese, Canada. J Food Prot 81(2):325–331. https://doi.org/10.4315/0362-028X.JFP-17-283
doi: 10.4315/0362-028X.JFP-17-283
McCollum JT, Williams NJ, Beam SW, Cosgrove S, Ettestad PJ, Ghosh TS, Kimura AC, Nguyen L, Stroika SG, Vogt RL et al (2012) Multistate outbreak of Escherichia coli O157:H7 infections associated with in-store sampling of an aged raw-milk Gouda cheese, 2010. J Food Prot 75(10):1759–1765. https://doi.org/10.4315/0362-028X.JFP-12-136
doi: 10.4315/0362-028X.JFP-12-136 pubmed: 23043823
Lewis K, Vasser M, Garman K, Higa J, Needham M, Irving D J, Cavallo S, Marks DS, Kirchner M, Madad A et. al. (2023) Notes from the Field: Multistate, Multiserotype Outbreak of Salmonella Infections Linked to Cashew Brie - United States, 2021. MMWR. Morb Mortal Wkly Rep 72(21):589–590. https://doi.org/10.15585/mmwr.mm7221a4
Praça J, Furtado R, Coelho A, Correia CB, Borges V, Gomes JP, Pista A, Batista R (2023) Listeria monocytogenes, Escherichia coli and Coagulase Positive Staphylococci in Cured Raw Milk Cheese from Alentejo Region. Portugal Microorganisms 11(2):322. https://doi.org/10.3390/microorganisms11020322
doi: 10.3390/microorganisms11020322 pubmed: 36838288
Poolman JT, Wacker M (2016) Extraintestinal pathogenic Escherichia coli, a common human pathogen: challenges for vaccine development and progress in the field. J Infect Dis 213(1):6–13. https://doi.org/10.1093/infdis/jiv429
doi: 10.1093/infdis/jiv429 pubmed: 26333944
Campos de ACLP, Puño-Sarmineto JJ, Medeiros LP, Gazal LES, Maluta RP, Navarro A, Kobayashi RKT, Fagan EP, Nakazato G (2018) Virulence genes and antimicrobial resistance in Escherichia coli from cheese made from unpasteurized milk in Brazil. Foodborne Pathog Dis 15:94–100. https://doi.org/10.1089/fpd.2017.2345
Guzman-Hernandez R, Contreras-Rodriguez A, Hernandez-Velez R, Perez-Martinez I, Lopez-Merino A, Zaidi MB, Estrada-Garcia T (2016) Mexican unpasteurized fresh cheeses are contaminated with Salmonella, non-O157 Shiga toxin producing Escherichia coli and potential uropathogenic E. coli strains: A public health risk. Int Food Microb 237:10–16. https://doi.org/10.1016/j.ijfoodmicro.2016.08.018
doi: 10.1016/j.ijfoodmicro.2016.08.018
Ribeiro LF, Barbose MM, Pinto FR, Maluta RP, Oliveira MC, de Souza V, de Medeiros MI, Borges LA, do Amaral LA, Fairbrother JM (2016) Antimicrobial resistance and virulence factors of Escherichia coli in cheese made from unpasteurized milk in three cities in Brazil. Foodborne Pathog Dis 13(9), 469–476. https://doi.org/10.1089/fpd.2015.2106
Wasiński B. Extra-intestinal pathogenic Escherichia coli–threat connected with food-borne infections (2019) Ann Agric Environ Med 26(4):532–537. https://doi.org/10.26444/aaem/111724 .
Maluta RP, Logue CM, Casas MR, Meng T, Guastalli EA, Rojas TC, Montelli AC, Sadatsune T, de Carvalho RM, Nolan LK et al (2014) Overlapped sequence types (STs) and serogroups of avian pathogenic (APEC) and human extra-intestinal pathogenic (ExPEC) Escherichia coli isolated in Brazil. PLoS ONE 9(8):e105016. https://doi.org/10.1371/journal.pone.0105016
doi: 10.1371/journal.pone.0105016 pubmed: 25115913 pmcid: 4130637
Aworh MK, Kwaga JKP, Hendriksen RS, Okolocha EC, Thakur S (2021) Genetic relatedness of multidrug resistant Escherichia coli isolated from humans, chickens and poultry environments. Antimicrob Resist Infect Control 10(1):58. https://doi.org/10.1186/s13756-021-00930-x
doi: 10.1186/s13756-021-00930-x pubmed: 33757589 pmcid: 7988975
Zhuge X, Zhou Z, Jiang M, Wang Z, Sun Y, Tang F, Xue F, Ren J, Dai J (2021) Chicken-source Escherichia coli within phylogroup F shares virulence genotypes and is closely related to extraintestinal pathogenic E. coli causing human infections. Transbound Emerg Dis 68(2):880–895. https://doi.org/10.1111/tbed.13755
doi: 10.1111/tbed.13755 pubmed: 32722875
Homeier-Bachmann T, Kleist JF, Schütz AK, Bachmann L (2022) Distribution of ESBL/AmpC-Escherichia coli on a Dairy Farm. Antibiotics (Basel) 11(7):940. https://doi.org/10.3390/antibiotics11070940
doi: 10.3390/antibiotics11070940 pubmed: 35884193
O’Neill J. Tackling drug-resistant infections globally: final report and recommendations The Review on antimicrobial resistance. May 2016. https://amr-review.org/sites/default/files/160518_Final%20paper_with%20cover.pdf . Accessed 27 March 2024
Kamaruzzaman EA, Abdul Aziz S, Bitrus AA, Zakaria Z, Hassan L (2020) Occurrence and characteristics of extended-spectrum β-Lactamase-producing Escherichia coli from dairy cattle, milk, and farm environments in Peninsular Malaysia. Pathogens 9(12):1007. https://doi.org/10.3390/pathogens9121007
doi: 10.3390/pathogens9121007 pubmed: 33266299 pmcid: 7760176
Brown K, Mugoh M, Call DR, Omulo S (2020) Antibiotic residues and antibiotic-resistant bacteria detected in milk marketed for human consumption in Kibera. Nairobi PLoS One 15(5):e0233413. https://doi.org/10.1371/journal.pone.0233413
doi: 10.1371/journal.pone.0233413 pubmed: 32463823
Tóth AG, Csabai I, Krikó E, Tőzsér D, Maróti G, Patai AV, Makrai L, Szita G, Solymosi N (2020) Antimicrobial resistance genes in raw milk for human consumption. Sci Rep 10(1):7464. https://doi.org/10.1038/s41598-020-63675-4
doi: 10.1038/s41598-020-63675-4 pubmed: 32366826 pmcid: 7198526
Dos Santos Rosario AIL, da Silva MY, Castro VS, da Silva MCA, Conte-Junior CA, da Costa MP (2021) Everybody loves cheese: crosslink between persistence and virulence of Shiga-toxin Escherichia coli. Crit Rev Food Sci Nutr 61(11):1877–1899. https://doi.org/10.1080/10408398.2020.1767033
doi: 10.1080/10408398.2020.1767033 pubmed: 32519880

Auteurs

Rita Mendonça (R)

Department of Food and Nutrition, National Institute of Health Doutor Ricardo Jorge, Lisbon, Portugal. riitamendonca@gmail.com.
Faculty of Sciences, University of Lisbon, Lisbon, Portugal. riitamendonca@gmail.com.

Rosália Furtado (R)

Department of Food and Nutrition, National Institute of Health Doutor Ricardo Jorge, Lisbon, Portugal.

Anabela Coelho (A)

Department of Food and Nutrition, National Institute of Health Doutor Ricardo Jorge, Lisbon, Portugal.

Cristina Belo Correia (CB)

Department of Food and Nutrition, National Institute of Health Doutor Ricardo Jorge, Lisbon, Portugal.

Elena Suyarko (E)

Department of Infectious Diseases, National Institute of Health Doutor Ricardo Jorge, Lisbon, Portugal.
NOVA School of Science and Technology, 2829-516, Caparica, Portugal.

Vítor Borges (V)

Department of Infectious Diseases, National Institute of Health Doutor Ricardo Jorge, Lisbon, Portugal.

João Paulo Gomes (JP)

Department of Infectious Diseases, National Institute of Health Doutor Ricardo Jorge, Lisbon, Portugal.
Animal and Veterinary Research Center (CECAV), Faculty of Veterinary Medicine, Lusófona University-Lisbon University Centre, Lisbon, Portugal.

Angela Pista (A)

Department of Infectious Diseases, National Institute of Health Doutor Ricardo Jorge, Lisbon, Portugal.

Rita Batista (R)

Department of Food and Nutrition, National Institute of Health Doutor Ricardo Jorge, Lisbon, Portugal. rita.batista@insa.min-saude.pt.

Classifications MeSH