Contamination by antibiotic-resistant bacteria in foods: the danger of eating ready-to-eat vegetables
DOI:
https://doi.org/10.33448/rsd-v11i10.33099Keywords:
Bacteria; Antibiotic-Resistant; Ready to eat vegetables.Abstract
Introduction: The heavy tendencie to purchase ready for consumption vegetables in the last years, has been significantly assossiated to infection outbreaks and food poisoning. These ingredients are potentially contamined by pathogenic microorganisms and the greatest concern refers to human exposition to resistant antimicrobial agents, which encoraged the researchers to study many forms of resistant strains in food. Objective: The purpose of this study was to elucidate the contamination of ready for consumption vegetables with antibiotic resistant bacteria and the risks of its consumption. Methodology: It's a narrative review on existing literature that aimed to clarify the risks of ingestion of ready for consumption vegetables due to its contamination with antibiotic resistant bacteria. The research was made through online access to the following database: Google Scholar, National Library of Medicine (PubMed MEDLINE), Scientific Electronic Library Online (Scielo), Biblioteca Virtual em Saúde (BVS). Results and discussion: In all of the 25 articles researched, resistant bacteria were found. Of the total, 86,51% of the bacteria were resistan to at least one antibiotic. Of the bacteria which showed resistance, 76,92 % were resistant to at least 5 antibiotics and 44,23% were resistant to over 10 antibiotics. Conclusion: The present study demonstrates that ready for consumption vegetables have a large microbiota with different genus of bacteria, the majoritt of which antibiotic resistant.
References
Abakari, G., Cobbina, S. & Yeleliere, E. (2018). Microbial quality of ready-to-eat vegetable salads vended in the central business district of Tamale, Ghana. International Journal of Food Contamination, 5(3): 1–9.
Abriouel, H., Omar, N. B., Molinos, A. C., Lopez, R. L., Jose Grande, M., MartinezViedma, P. et al. (2008). Comparative analysis of genetic diversity and incidence of virulence factors and antibiotic resistance among enterococcal populations from raw fruit and vegetable foods, water and soil, and clinical 265 samples. International Journal of Food Microbiology, 123, 38–49.
Al Mamun M., Rahman, S. M. M. & Turin, T. C. (2013) Microbiological Quality of Selected Street Food Items Vended by School-Based Street Food Vendors in Dhaka, Bangladesh. Int J Food Microbiol 166:413–8.
Baran, A., Adigüzel, M. C., & Aydin, H. (2022). Microbiological quality of ready-to-eat vegetable salads served at meat restaurants under the COVID 19 pandemic induced food demand: an example from Eastern Turkey. Research Square. doi:10.21203/rs.3.rs-1736848/v1.
Barton Behravesh, C., Mody, R. K., Jungk, J., Gaul, L., Redd, J. T. & Chen, S. (2011) Outbreak of Salmonella saintpaul infections associated with raw produce. New England Journal of Medicine, 364, 918e927.
Bernardo, R., Duarte, A., Tavares, L., Barreto, A. S., Henriques, A. R. (2021). Listeria monocytogenes Assessment in a Ready-to-Eat Salad Shelf-Life Study Using Conventional Culture-Based Methods, Genetic Profiling, and Propidium Monoazide Quantitative PCR. Foods, 10, 235.
Blair, J. M. et. al.(2015). Molecular Mechanisms of Antibiotic Resistance. Nature, v. 13, p. 42-51.
Brasil, Ministério da Saúde. Portaria GM/MS nº 3.398, 7 de dezembro de 2021. Diário Oficial da União. seção 1. p.59.
Buchholz, U., Bernard, H., Werber, D., Beohmer, M. M., Remschmidt, C. & Wilking, H. (2011). German outbreak of Escherichia coli associated with sprouts. New England Journal of Medicine, 365, 1763e1770.
Campos, J., Mourão, J., Pestana, N., Peixe, L., Novais, C. & Antunes, P. (2013). Microbiological quality of ready-to-eat salads: An underestimated vehicle of bacteria and clinically relevant antibiotic resistance genes, International Journal of Food Microbiology, Volume 166, Issue 3, Pages 464-470.
Candel, F. J., Lopez, R., Valdivia, A., Nunes, M. J., Roca-Arbones, V. & Picazo De La Garza, J. J. (2002). Endocarditis due to Stenotrophomonas maltophilia. Enferm. Infecc. Microbiol. Clin, 20-477-8.
Carrasco, E., Morales-Rueda, A., & García-Gimeno, R. M. (2012). Cross-contamination and recontamination by Salmonella in foods: A review. Food Research International, 45(2), 545–556.
Carrilho, C. M. D. M., Grion, C. M. C., Bonametti, A. M., Medeiros, E. A. S. & Matsuo, T. (2007). Multivariate analysis of the factors associated with the risk of pneumonia in intensive care units. The Brazilian Journal of Infectious Diseases, Salvador, v. 11, n. 3, p.339-344.
Castrica, M., Andoni, E., Curone, G., Copelotti, E., Massacci, F. R., Terio, V., Colombo, S. & Balzaretti, C.M. (2021). Prevalence of Listeria monocytogenes and Salmonella spp. in Different Ready to Eat Foods from Large Retailers and Canteens over a 2-Year Period in Northern Italy. Int. J. Environ. Res. Public Health, 18, 10568.
Castro-Ibáñez, I., Gil, M.I. & Allende, A. (2017). A. Ready-to-eat vegetables: Current problems and potential solutions to reduce microbial risk in the production chain. LWT-Food Sci. Technol. 85, 284–292.
Castro-Rosas, J., Cerna-Cortes, J. F., Mendez-Reyes, E., Lopez-Hernandez, D., Gomez-Aldapa, C. A. & Estrada-Garcia, T. (2012). Presence of faecal coliforms, Escherichia coliand diarrheagenice. colipathotypes inready-to-eat salads, from an area where crops are irrigatedwith untreated sewage water.Int J Food Microbiol, 156:176–180.
Chajęcka-Wierzchowska, W., Zarzecka, U. & Zadernowska, A. (2021). Enterococci isolated from plant-derived food - analysis of antibiotic resistance and the occurrence of resistance genes. LWT - Food Sci. Technol. (Lebensmittel-Wissenschaft -Technol.), 139, p. 110549.
Chantziaras, I., Boyen, F., Callens, B. & Dewulf, J. (2014). Correlation Between Veterinary Antimicrobial Use and Antimicrobial Resistance in Food-Producing Animals: A Report on Seven. J Antimicrobial Chem. 69(3):827–34.
Collignon, P., Aarestrup, F. M., Irwin, R. & McEwen, S. (2013). Human Deaths and Thirdgeneration Cephalosporin Use in Poultry. Europe Emerg Infect Dis 19:1339–40.
Daniels, A. O., Jolapamo, O., Temikotan, T., & Akinkugbe, A. O. (2019). Resistance Profile of Contaminating Organisms Isolated From Ready-to-Eat Vegetable Salad From Selected Eateries in a University Setting. International Journal of Development Research. Vol. 09, Issue, 10, pp. 30247-30252.
Desai, P. T., Porwollik, S., Long, F., Cheng, P., Wollam, A. et al. (2013). Evolutionary genomics of Salmonella enterica subspecies. mBio, 4(2). e00579-12.
Devides, G., Gianini, G., Maffei, D. F. & Catanozi, M. P. L. M., (2014). Perfil socioeconômico e profissional de manipuladores de alimentos e o impacto positivo de um curso de capacitação em Boas Práticas de Fabricação. Brazilian Journal Of Food Technology, v. 17, n. 2, p.166-176.
Dietrich, R., Jessberger, N., Ehling-Schulz, M., Märtlbauer, E. & Granum, P.E. (2021). The Food Poisoning Toxins of Bacillus cereus. Toxins, 13, 98.
Ema, F. A., Shanta, R. N., Rahman, M., Islam, M., & Khatun, M. (2022). Isolation, identification, and antibiogram studies of Escherichia coli from ready-to-eat foods in Mymensingh, Bangladesh. Veterinary World, 15(6).
Enabulele, S. & Ehiabhi, G. (2020). Characterisation of Multi-drug Resistant Salmonella spp. Isolated From Ready to Eat Vegetable Salads Using The 16S rRNA Sequence Analysis. Journal of Basic and Applied Sciences 5(1): 97 – 112.
Eruteya, O. C. (2018). Occurrence and Antibiotic Susceptibility of Listeria Species Isolated from Ready-to-eat Mixed Vegetable Salad Sold in Fast Food Eateries in Port Harcourt. Methodology. International Journal of Pathogen Research, 5(3), 1-7.
Eze, N. M., Maduabum, F. O., Onyeke, N. G., Anyaegunam, N. J., Ayogu, C. A., Ezeanwu, B. A., et al. (2017). Awareness of food nutritive value and eating practices among Nigerian bank workers: Implications for nutritional counseling and education. Medicine, 96(10), Article e6283.
Falomir, M. P., Gozalbo, D., & Rico, H. (2010). Coliform bacteria in fresh vegetables: from cultivated lands to consumers. Current research, technology and education topics in applied microbiology and microbial biotechnology, 2, 1175-1181.
Fiedler, G., Schneider, C., Igbinosa, E. O., Kabisch, J., Brinks, E., Becker, B. & Franz, C. M. (2019). Antibiotics resistance and toxin profiles of Bacillus cereus-group isolates from fresh vegetables from German retail markets. BMC microbiology, 19(1), 1-13.
Food and Agriculture Organization of the United Nations (FAO) (2015). Status Report on Antimicrobial Resistance. Rome: Food and Agriculture Organization of the United Nations.
Ieren, I., I., Bello, M. & Kwaga, J. K. (2013). Occurrence and antibiotic resistance profile of Listeria monocytogenes in salad vegetables and vegetable salads sold in Zaria, Nigeria. Afr. J. Food Sci. 7: 334 – 338.
Ilyas, S., Qamar, M.U., Rasool, M.H., Abdulhaq, N. & Nawaz, Z. (2016). Multidrug-resistant pathogens isolated from RTE salads available at a local market in Pakistan. Brit Food J, 118, 2068–2075.
Internacional Fresh-Cut Produce Association - IFPA. (2007).
Iseppi,. R., de Niederhäusern, S., Bondi, M., Messi, P. & Sabia, C. (2018) Extended-Spectrum blactamase, AmpC, and MBL-Producing Gram-Negative Bacteria on Fresh Vegetables and Ready-to-Eat Salads Sold in Local Markets. Microb Drug Resist. 24:1156–64.
Johnston, L. M. & Jaykus, L. A. (2004) Antimicrobial resistance of Enterococcus species isolated from produce. Appl Environ Microbiol, 70: 3133–3137.
Karikari, A. B., Kpordze, S. W., Yamik, D. Y., & Saba, C. S. (2022). Ready-to-Eat Foods as sources of Extended Spectrum β-lactamase producing Salmonella and E. coli in Tamale, Ghana. Frontiers in Tropical Diseases, 15.
Kochakkhani, H., Dehghan, P., Mousavi, M.H. and Sarmadi, B. (2016). Occurrence, molecular detection and antibiotic resistance profile of Escherichia coli O157:H7 isolated from ready-to-eat vegetable salads in Iran. Pharmaceutical Sciences, Vol. 22 No. 3, pp. 195-202.
Koushki, M.; Koohy-Kamaly, P.; Sohrabvandi, S.; Mehrabi, S. (2021) Assessment of the Microbial Quality of Industrial Ready-to-Eat Salads Containing Meat Products. Curr. Res. Nutr. Food Sci., 9, 662–670.
Lee, T. S., Lee, S. W., Seok, W. S., Yoo, M. Y., Yoon, J. W., Park, B. K., & Oh, D. H. (2004). Prevalence, antibiotic susceptibility, and virulence factors of Yersinia enterocolitica and related species from ready-to-eat vegetables available in Korea. Journal of food protection, 67(6), 1123-1127.
Macdonald, E., Heier, B. T., Nygard, K., Stalheim, T., Cudjoe, K.S. & Skjerdal, T. (2012). Yersinia enterocolitica outbreak associated with ready-to-eat salad mix, Norway. Emerging Infectious Diseases, 18, 1496e1499.
Manyi-Loh, C., Mamphweli, S., Meyer, E., Okoh, A. (2018). Antibiotic use in agriculture and its consequential resistance in environmental sources: Potential public health implications. Molecules, 23(4), 795.
Mir, S.A., Shah, M.A., Mir, M.M., Dar, B.N., Greiner, R. and Roohinejad, S. (2018) Microbiological contamination of RTE vegetable salads in developing countries and potential solutions in the supply chain to control microbial pathogens. Food Control. 85, 235–244.
Mohamed, S.A., Ardiyati, T., Rifa’i, M. & Widodo,(2020). Detection of class 1 integron-associated gene cassettes and tetracycline resistance genes in Escherichia coli isolated from ready to eat vegetables, Annals of Medicine and Surgery, Volume 55, Pages 327-331.
Mohammed, B., & Muhammad, A. U. (2020). Antibiotic resistance patterns of salmonella typhi isolated from ready-to-eat vegetable salads hawked in Kano Metropolis. Bayero. Journal of Pure and Applied Sciences. 12(2), 74-80.
Mozaffarian, D., Angell, S. Y., Lang, T., & Rivera, J. A. (2018). Role of government policy in nutrition—barriers to and opportunities for healthier eating. BMJ, 361, k2426.
Nguyen, T. T., Huong, N. M., Pham, T. L., Le Thi, H. H., & Ta, T. Y. (2020). Isolation and Identification of β-Lactamase Producing Pseudomonas spp. in Ready-To-Eat Raw Vegetables. Health Risk Analysis, (1), 101-107.
Normanno, G., Corrente, M., La Salandra, G., Dambrosio, A., Quaglia, N. C. et al. (2007). Methicillin-resistant Staphylococcus aureus (MRSA) in foods of animal origin product in Italy. International Journal of Food Microbiology, Amsterdam, v. 117, n. 2, p. 219-222.
Noor, R. (2016). Microbiological Quality of Commonly Consumed Street Foods in Bangladesh. Nutr Food Sci, 46(1):130–41.
Okafor‐Elenwo, E. J., & Imade, O. S. (2020). Ready‐to‐eat vegetable salads served in Nigerian restaurants: a potential source of multidrug‐resistant bacteria. Journal of Applied Microbiology, 129(5), 1402-1409.
Osterblad, M., Hakanen, A., Manninen, R., Leistevuo, T., Peltonen, R. et al. (2000). A between-species comparison of antimicrobial resistance in enterobacteria in fecal flora. Antimicrob Agents Ch.44(6):1479–84.
Perera, N., Gamage, T., Wakeling, L., Gamlath, G. & Versteeg, C. (2010). Colour and texture of apples high pressure processed in pineapple juice. Innovative Food Science & Emerging Technologies. 11(1), 39e46.
Phillips, I., Casewell, M., Cox, T., De Groot, B., Friis, C. et al. (2004). Does the use of antibiotics in food animals pose a risk to human health? Journal of Antimicrobial Chemotherapy, London, v. 53, n. 1, p. 28-52.
Rico, H., & Falomir, P. (2020). Comparison of the Antibiotic-Resistant Enterobacteriaceae Content in Conventional, Organic and Fresh-Cut Vegetables Sold in Valencia (Spain). AIMS Agriculture and Food, 5(2), 233-244.
Rother, E. T. (2007). Revisão sistemática X revisão narrativa. Acta paul. enferm. Jun; 20(2):1-2.
Ruíz-Cruz, S., Felix, E. A., Cinco, M. D., Osuna, M. A. I. & Aguilar, G. A. G. (2007). Efficacy of sanitizers in reducing Escherichia coli O157:H7, Salmonella spp. And Listeria monocytogenes populations on fresh-cut carrots. Food Control. 18(11),1383e1390
Şanlıbaba, P., Tezel, B. U., & Çakmak, G. A. (2018). Prevalence and antibiotic resistance of Listeria monocytogenes isolated from ready-to-eat foods in Turkey. Journal of Food Quality. Volume 2018, Article ID 7693782, 9 pages.
Sapkota, S., Adhikari. S., Pandey, A., Khadka, S., Adhikari, M., Kandel, H. et al. (2019). Multi-drug resistant extended-spectrum beta-lactamase producing E. coli and Salmonella on raw vegetable salads served at hotels and restaurants in Bharatpur, Nepal. BMC Res Notes, 12(1):516.
Schwaiger, K., Helmke, K., Hölzel, C.S. & Bauer, J. (2011). Antibiotic resistance in bacteria isolated from vegetables with regards to the marketing stage (farm vs. supermarket), International Journal of Food Microbiology, Volume 148, Issue 3Pages 191-196.
Sultana, A. et al. (2013). Sanitation Practices Among Food Handlers Working in Street Restaurants in Rawalpindi, Pakistan. Rawal Medical Journal, Pakistan; v. 38, n. 4, p. 425- 427.
Sousa, L. M. M.; Firmino, C. F.; Marques-Vieira, C. M. A.; Severino, S. S. P. & Pestana, H. C. F. C. (2018). Revisões da literatura científica: tipos, métodos e aplicações em enfermagem. Revista Portuguesa de Enfermagem de Reabilitação, 1(1), 45–54.
Souza, P. S., Feijó, M. B. S. & Marin, V. A. (2013). Doenças crônicas e a internalização de microorganismos patogênicos. Higiene dos Alimentos. 27(226/227): 90-94.
Tavakoli-Far, B., Mousavi, B., Mashak, Z., Rezaei, M. A., Doregiraee, F., Kachoie, M. A., & Jafari-Eskari, S. (2020). Molecular Typing and Phenotypic and Genotypic Evaluation of Antibiotic Resistance and Virulence Factors of the Methicillin-Resistant Staphylococcus Aureus Bacteria Isolated From Vegetable and Salad Samples. Research Square. doi: 10.21203/rs.3.rs-116662/v1.
Toe, E., Attien, P., Aboya, J. L. M., Sina, H., Kouame, D. N. K., Kamnire, O. & Adjehi, T. D. (2022). Prevalence and characterization of Salmonella isolated from vegetables salads and ready to eat raw mixed vegetable salads in Abidjan, Côte d’Ivoire. Journal of Microbiology and Antimicrobials, 14(1), 15-25.
Tomasi, N., Pinton, R., Dalla Costa, L., Cortella, G., Terzano, R.., Mimmo, T., Scampicchio, M. & Cesco, S. (2015). New ‘solutions’ for floating cultivation system of ready-to-eat salad: A review. Trends Food Sci. Technol. 46, 267–276.
Vietnam food safety risks management: challenges and opportunities. (2017). Technical working paper. Hanoi, Vietnam: The World Bank. Available at: http://documents.worldbank.org/ curated/en/415551490718806138/technical-working-paper (04.01.2020).
World Health Organization (WHO) (2015a). Global Action Plan on Antimicrobial Resistance. Geneva.
Yang, X., Huang, J., Zhang, Y., Liu, S., Chen, L., Xiao, C. et al. (2020). Prevalence, abundance, serovars and antimicrobial resistance of Salmonella isolated from retail raw poultry meat in China. The Science of the Total Environment, 713, 136385.
Yang, X., J. Huang, J., Wu, Q., Zhang,J., Yang, S., Wang, J. et al. (2022). Occurrence, serovars and antibiotic resistance of Salmonella spp. in retail ready-to-eat food products in some Chinese provinces. LWT-Food Science and Technology, 154, Article 112699.
Yu, S., Cong, X., Su, Y., & Huang, X. (2010). Investigation and analysis on food poisoning caused by Salmonella contaminated cold dish. Occupation and Health, 26(8), 879–881.
Zhang, S., Huang, Y., Yang,G.; Lei, T., Chen, M.,et al. (2021). High prevalence of multidrug-resistant Escherichia coli and first detection of IncHI2/IncX4-plasmid carrying mcr-1 E. coli in retail ready-to-eat foods in China, International Journal of Food Microbiology, Volume 355, 109349.
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