Good Manufacturing Practices of butcher shops and frequency of Shiga toxin-producing Escherichia coli and Salmonella spp. from ground meat from butcher shops in Asunción, Paraguay
DOI:
https://doi.org/10.18004/mem.iics/1812-9528/2024.e22122402Keywords:
Hygienic-sanitary quality, Butcher shops, Hygienic-sanitary quality, Butcher shops, STEC, Salmonella, SalmonellaAbstract
The safety of marketed meat must be guaranteed in the production chain, to avoid foodborne illness. Shiga toxin-producing Escherichia coli (STEC) and Salmonella spp. can be found in the gastrointestinal tract of cattle and contaminate meat for human consumption, potentially causing diseases in humans. This work aimed to evaluate the hygienic-sanitary conditions of 52 butcher shops located in Asunción and detect the frequency of STEC and Salmonella spp. in ground beef samples. Hygienic-sanitary conditions were evaluated by estimating risk, using a categorical classification scale. The detection of STEC and Salmonella spp. was performed by real-time PCR. In the initial evaluation, 33% of the butcher shops were classified as high and moderate risk. STEC non-O157 was detected in 50% (130/258) of the samples and Salmonella spp. in 11% (29/258). Improvement actions were carried out. In the post-intervention stage, no high-risk butcher shops were detected. In the follow-up sampling, 29% (66/237) of positive samples were detected for STEC non-O157 and 7% (16/237) for Salmonella spp. This study allowed specific and detailed recommendations to be made to each butcher shop, which had a significant effect on improving their conditions. This situation highlights the importance of continuing to strengthen multisectoral and multidisciplinary surveillance. It is imperative that establishments dedicated to the sector implement Good Manufacturing Practices (GMP) as a measure to reduce associated risks.
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References
Naciones Unidas. Los alimentos contaminados cuestan 420.000 vidas y 95.000 millones de dólares en pérdidas al año. Noticias ONU [Internet]. [acceso 19 de junio de 2023]. 2022. https://news.un.org/es/story/2022/06/1509842
Laino LD, Laino I, Musálem K, Laino LD, Laino I, Musálem K. Comercio Internacional y Competitividad de la Producción Ganadera en Paraguay. Poblac Desarro [Internet]. 2018 [acceso 12 de julio de 2023]; 24 (46): 99-109. http://scielo.iics.una.py/scielo.php?script=sci_abstract&pid=S2076-054X2018004600099&lng=en&nrm=iso&tlng=es
Brusa V, Costa M, Londero A, Leotta G Galli L.. Characterization and Molecular Subtyping of Shiga Toxin-Producing Escherichia coli Strains in Butcher Shops. Foodborne pathogens and disease. 2017; 14(5),253-259. https://doi.org/10.1089/fpd.2016.2238
Ruiz MJ, Padola N, Leotta G, Colello R, Passucci J, Rodríguez E, et al. Calidad microbiológica de la carne picada y detección de patógenos en muestras ambientales de carnicerías de la ciudad de Tandil, provincia de Buenos Aires, Argentina. Revista Argentina de microbiología. 2022; 54(3): 215-219. https://doi.org/10.1016/j.ram.2021.04.003
Costa M, Pracca G, Sucari A, Galli L, Ibargoyen J, Gentiluomo J, et al. Comprehensive evaluation and implementation of improvement actions in bovine abattoirs to reduce pathogens exposure. Prev Vet Med. 2020; 176. https://doi.org/10.1016/j.prevetmed.2020.104933
González T, Rojas R. Enfermedades transmitidas por alimentos y PCR: prevención y diagnóstico [Internet]. 2005 [acceso 12 de julio de 2023]; 47(5): 388-390. https://www.scielo.org.mx/scielo.php?script=sci_arttext&pid=S0036-36342005000500010
Torso L, Voorhees R, Forest S, Gordon A, Silvestri S, Kissler B, et al. Escherichia coli O157:H7 Outbreak Associated with Restaurant Beef Grinding. Journal of food protection 2015; 78(7),1272-1279. https://doi.org/10.4315/0362 028X.JFP-14-545
Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, et al. Foodborne Illness Acquired in the United States-Major Pathogens. Emerg Infect Dis [Internet]. 2011 [acceso 12 de julio de 2023]; 17(1): 7-15. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3375761/
Martínez-Chávez L, Cabrera-Diaz E, Pérez-Montaño JA, Garay-Martínez LE, Varela-Hernández JJ, Castillo A, et al. Quantitative distribution of Salmonella spp. and Escherichia coli on beef carcasses and raw beef at retail establishments. International Journal of Food Microbiology. 2015; 210:149-155. https://doi.org/10.1016/j.ijfoodmicro.2015.06.016
Municipalidad de Asunción. Observaciones para el transporte y comercialización de carne y menudencias para consumo humano. [Internet]. [acceso 12 de julio de 2023]. 2002. https://www.asuncion.gov.py/wp-content/uploads/2016/04/ORD-2002-27.pdf
Leotta GA, Brusa V, Galli L, Adriani C, Linares L, Etcheverría A, et al. Comprehensive Evaluation and Implementation of Improvement Actions in Butcher Shops. PloS One. 2016;11(9): e0162635. https://doi.org/10.1371/journal.pone.0162635
Laboratory Guidebook Notice of Change. Primer and Probe Sequences and Reagent Concentrations for non-O157 Shiga Toxin-Producing Escherichia coli (STEC) Real-Time PCR Assay. Laboratory Guidebook-USDA. 2019 [Internet] [acceso 20 de enero de 2024]. https://www.fsis.usda.gov/sites/default/files/media_file/2021-03/mlg-5-appendix-4.pdf
United States Department of Agriculture Food Safety and Inspection Service Isolation and Identification of Salmonella from Meat, Poultry, Pasteurized Egg, and Siluriformes (Fish) Products and Carcass and Environmental Sponges. Laboratory Guidebook-USDA. 2019 [Internet] [acceso 20 de enero de 2024]. https://www.fsis.usda.gov/sites/default/files/media_file/documents/MLG-4.13.pdf
Leotta GA, Chinen I, Epszteyn S, Miliwebsky E, Melamed IC, Motter M, et al. Validación de una técnica de PCR múltiple para la detección de Escherichia coli productor de toxina Shiga. Rev Argent Microbiol [Internet]. 2005 [acceso 12 de julio de 2023]; 37(1): 1-10. ISSN 0325-7541 ISSN 0325-7541 http://www.scielo.org.ar/scielo.php?script=sci_abstract&pid=S0325-75412005000100001&lng=es&nrm=iso&tlng=en
Grimont P. Antigenic Formulae of the Salmonella serovars, (9th ed.) Paris: WHO Collaborating Centre for Reference and Research on Salmonella. 2019 [acceso 22 de enero de 2024]. https://www.academia.edu/20495783/Antigenic_Formulae_of_the_Salmonella_serovars_9th_ed_Paris_WHO_Collaborating_Centre_for_Reference_and_Research_on_Salmonella
Sánchez Turcios RA. t-Student: Usos y abusos. Rev Mex Cardiol [Internet]. 2015 [acceso 23 de enero 2024]; 26(1): 59-61. ISSN: 0188-2198. http://www.scielo.org.mx/scielo.php?script=sci_abstract&pid=S0188-21982015000100009&lng=es&nrm=iso&tlng=es
Barril PA, Soto SA, Jaureguiberry MV, Gottardi G, Bascur I, Leotta GA, et al. Microbiological risk characterization in butcher shops from the province of Neuquen, Patagonia Argentina. LWT [Internet]. 2019 [acceso 12 de julio de 2023];107: 35-40. DOI: 10.1016/j.lwt.2019.02.074. https://www.sciencedirect.com/science/article/pii/S0023643819301707
Casas D, Brashears MM, Miller MF, Inestroza B, Bueso-Ponce M, Huerta-Leidenz N, et al. In-Plant Validation Study of Harvest Process Controls in Two Beef Processing Plants in Honduras. J Food Prot. 2019;82(4):677-83. https://doi.org/10.4315/0362-028X.JFP-18-395
Brusa V, Restovich V, Galli L, Arias R, Linares L, Costa M, et al. Reduction of Shiga toxin-producing Escherichia coli in a beef abattoir. Food Sci Technol Int [Internet]. 2022 [acceso 12 de julio de 2023]; 28(1): 50-9. https://doi.org/10.1177/1082013221991258
Rojas N, Martinez A, Acuña P, Rodriguez F, Padola N, Guillen R. Detection of Shiga Toxin-producing Escherichia coli in Ground Beef: Evaluation of Contamination Levels in Butcheries of The Metropolitan Zone in Asuncion, Paraguay [Internet]. Journal of Pure and Applied Microbiology. 2019 [acceso 12 de julio de 2023]. doi:10.22207/JPAM.13.1.08
Abu Bakar S, Radu S, Mahyudin NA, Rukayadi Y, Tuan Chilek TZ. Prevalence of Salmonella spp. in chicken and beef from retail outlets in Malaysia. Int Food Res J [Internet]. 2017 [acceso 12 de julio de 2023]; 24(1): 437-49. http://www.ifrj.upm.edu.my/24%20(01)%202017/(58).pdf
Boonmar S, Morita Y, Pulsrikarn C, Chaichana P, Pornruagwong S, Chaunchom S, et al. Salmonella prevalence in meat at retail markets in Pakse, Champasak Province, Laos, and antimicrobial susceptibility of isolates. J Glob Antimicrob Resist. 2013;1(3):157-61. https://doi.org/10.1016/j.jgar.2013.05.001
Santos PDM, Widmer KW, Rivera WL. PCR-based detection and serovar identification of Salmonella in retail meat collected from wet markets in Metro Manila, Philippines. PLOS ONE [Internet]. 2020 [acceso 12 de julio de 2023]; 15(9): e0239457. https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0239457
Phan TT, Khai LTL, Ogasawara N, Tam NT, Okatani AT, Akiba M, et al. Contamination of Salmonella in retail meats and shrimps in the Mekong Delta, Vietnam. J Food Prot. 2005;68(5): 1077-80. https://doi.org/10.4315/0362-028x-68.5.1077
Jure MA, Condorí S, Leotta GA, Chinen I, Miliwebsky E, Allori C, et al. Detección, aislamiento y caracterización de Escherichia coli productor de toxina Shiga a partir de carne molida fresca proveniente de carnicerías de Concepción, provincia de Tucumán. Rev Argent Microbiol [Internet]. 2010 [acceso 26 de julio de 2023]; 42(4): 284-7. ISSN: 0325-7541 ISSN: 0325-7541 http://www.scielo.org.ar/scielo.php?script=sci_abstract&pid=S0325-75412010000400009&lng=es&nrm=iso&tlng=es
United States Department of Agriculture. Food Safey and Inspection Service, Office of Public Health and Science. Detection, isolation and identification of Escherichia coli O157:H7 and O157: NM (nonmotile) from meat products. USA, 2002, p.1-13. Laboratory Guidebook-USDA. 2019 [Internet] [acceso 20 de enero de 2024]. https://www.fsis.usda.gov
United States Department of Agriculture. Food Safety and Inspection Service, Office of Public Health and Science. Detection, isolation and identification of Escherichia coli O157:H7 from meat products. MLG 5.04. USA, 2008. Laboratory Guidebook-USDA. 2019 [Internet] [acceso 20 de enero de 2024]. https://www.fsis.usda.gov
Brusa V, Aliverti V, Aliverti F, Ortega EE, de la Torre JH, Linares LH, et al. Shiga toxin-producing Escherichia coli in beef retail markets from Argentina. Front Cell Infect Microbiol. 2012; 2: 171. https://doi.org/10.3389/fcimb.2012.00171
Li MC, Wang F, Li F. Identification and molecular characterization of antimicrobial-resistant shiga toxin-producing Escherichia coli isolated from retail meat products. Foodborne Pathog Dis. 2011;8(4):489-93. https://doi.org/10.1089/fpd.2010.0688
Ortiz F, Weiler N, Alvarez M, Orrego MV, Kawabata A, Riera E, et al. Resistencia a múltiples antibióticos en serovariedades de Salmonella aisladas de muestras clínicas y alimentos. Mem Inst Investig En Cienc Salud [Internet]. 2021 [acceso 12 de julio de 2023]; 19(1): 37-47. ISSN 1812-9528. http://scielo.iics.una.py/scielo.php?script=sci_abstract&pid=S1812-95282021000100037&lng=en&nrm=iso&tlng=es
Alvarez F, Alvarez FL, Copes J, Alvarez M, Nuñez L, Suzuki K. Frecuencia de Salmonella enterica en aves de traspatio de la localidad de San Lorenzo, Departamento Central, República del Paraguay. Compend Cienc Vet 2012 02(01): 9-11. ISSN 0365-5148. http://www.vet.una.py/dict/pdf/ccv02/alvarez.pdf
Cardozo L, Álvarez M, Suzuki K, Giménez G, Weiler N, Leotta GA, et al. Estudio preliminar sobre el aislamiento y la identificación de Salmonella enterica en cerdos de la República del Paraguay. Analecta Vet [Internet]. 2010 [acceso 31 de julio de 2023];30, no1, número especial. ISSN: 0365-5148 ISSN: 0365-5148 http://sedici.unlp.edu.ar/handle/10915/96832
