Antimicrobial resistance of the microbiota of cheeses served in an oncology hospital in Rio de Janeiro-Brazil
DOI:
https://doi.org/10.33448/rsd-v11i12.34837Keywords:
Bacterial resistance; Food; Antimicrobial; Gram-negative bacteria; Hospital infection.Abstract
Bacterial resistance to antimicrobials is one of the major challenges for public health today. An important concern is food provided in a hospital environment, due to its ability to transmit antimicrobial resistance genes. This study aimed to evaluate antimicrobial resistance, and characterize the resistance genes of gram-negative bacteria in the microbiota of cheese samples served to patients admitted to a public hospital in Rio de Janeiro. This research used a methodology to capture the Gram-negative microbiota resistant to antimicrobials. The disk diffusion test and the polymerase chain reaction (PCR) were performed to investigate, respectively, the phenotypic and genotypic resistance of Gram-negative bacteria to the tested antimicrobials. The microbiota of all cheese samples showed high phenotypic resistance. In 62.5% of the samples, resistance reached more than nine tested antimicrobials. Five antimicrobials did not show susceptibility in 100% of the samples analyzed. With the exception of the antimicrobial ciprofloxacin, resistance percentages above 62% were found in all samples, including fourth-generation cephalosporin. All cheese samples harbored resistance genes. Seven different resistance genes were found in 34 microbiota of Gram-negative bacteria, namely: int-1, int-2, ctx, shv, tem, tetA and tetB. We conclude the alarming presence of potentially antimicrobial-resistant genes in cheeses served to cancer patients, indicating that this food may be a carrier of bacteria with resistance genes in a hospital environment.
References
Al-Ashmawy, M. A., Sallam, K. I., Abd-Elghany, S. M., Elhadidy, M., & Tamura, T. (2016). Prevalence, molecular characterization, and antimicrobial susceptibility of methicillin-resistant Staphylococcus aureus isolated from milk and dairy products. Foodborne Pathogens and Disease, 13(3), 156–162.
Ambler, R. P. (1980). The structure of β-lactamases. Philosophical Transactions of the Royal Society of London. B, Biological Sciences, 289(1036), 321–331.
Azimi, L., Rastegar-Lari, A., Talebi, M., Ebrahimzadeh-Namvar, A., & Soleymanzadeh-Moghadam, S. (2013). Evaluation of phenotypic methods for detection of Klebsiella pneumoniae carbapenemase-producing K. pneumoniae in Tehran. Journal of Medical Bacteriology, 2(3–4), 26–31.
Bacanlı, M., & Başaran, N. (2019). Importance of antibiotic residues in animal food. Food and Chemical Toxicology, 125, 462–466. https://doi.org/10.1016/j.fct.2019.01.033
Barros, R. R. (2021). Antimicrobial Resistance among Beta-Hemolytic Streptococcus in Brazil: An Overview. Antibiotics, 10(8), 973. https://doi.org/10.3390/antibiotics10080973
Secretaria de Vigilância em Saúde, Portaria no 64 de 11 de dezembro de 2018, Diário Oficial da União (2018). https://pesquisa.in.gov.br/imprensa/jsp/visualiza/index.jsp?data=14/12/2018&jornal=515&pagina=59
Brazilian Committee on Antimicrobial Susceptibility Testing. (2018). Termo de ratificação do acordo de cooperação técnico-científico do BrCAST 23-out-2018. http://brcast.org.br/documentos/
Brazilian Committee on Antimicrobial Susceptibility Testing/European Committee on Antimicrobial Susceptibility Testing. (2022). Tabela pontos de corte clínicos BrCAST 14-abr-2022. http://brcast.org.br/tabela-pontos-de-corte-clinicos-BrCAST-2017-final.pdf
Castanheira, M., Simner, P. J., & Bradford, P. A. (2021). Extended-spectrum β -lactamases: An update on their characteristics, epidemiology and detection. JAC-Antimicrobial Resistance, 3(3), dlab092. https://doi.org/10.1093/jacamr/dlab092
Cavaco, L., Mordhorst, H., & Hendriksen, R. (2016). Laboratory protocol: PCR for plasmid-mediated colistin resistance genes. Lyngby, Denmark: National Food Institute.
Centers for Disease Control and Prevention. (2009). Laboratory protocol for detection of carbapenem-resistant or carbapenemase-producing, Klebsiella spp. And E. coli from rectal swabs. Atlanta. GA: CDC.
Centers for Disease Control and Prevention. (2019). The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2017. EFSA Journal, 17(2), e05598. https://doi.org/10.2903/j.efsa.2019.5598
Cerceo, E., Deitelzweig, S. B., Sherman, B. M., & Amin, A. N. (2016). Multidrug-resistant gram-negative bacterial infections in the hospital setting: Overview, implications for clinical practice, and emerging treatment options. Microbial Drug Resistance, 22(5), 412–431.
Clinical and Laboratory Standards Institute. (2018). Performance standards for antimicrobial susceptibility testing. CLSI supplement M100.
Clinical and Laboratory Standards Institute. (2022). EM100 Connect—CLSI M100-ED32:2022. http://em100.edaptivedocs.net/GetDoc.aspx?doc=CLSI%20M100%20ED32:2022&scope=user
Collignon, P. (2013). The Importance of a One Health Approach to Preventing the Development and Spread of Antibiotic Resistance. Em J. S. Mackenzie, M. Jeggo, P. Daszak, & J. A. Richt (Orgs.), One Health: The Human-Animal-Environment Interfaces in Emerging Infectious Diseases: Food Safety and Security, and International and National Plans for Implementation of One Health Activities (p. 19–36). Springer. https://doi.org/10.1007/82_2012_224
da Silva Abreu, A. C., Matos, L. G., da Silva Cândido, T. J., Barboza, G. R., de Souza, V. V. M. A., Munive Nuñez, K. V., & Cirone Silva, N. C. (2021). Antimicrobial resistance of Staphylococcus spp. Isolated from organic and conventional Minas Frescal cheese producers in São Paulo, Brazil. Journal of Dairy Science, 104(4), 4012–4022. https://doi.org/10.3168/jds.2020-19338
Dallenne, C., Da Costa, A., Decré, D., Favier, C., & Arlet, G. (2010). Development of a set of multiplex PCR assays for the detection of genes encoding important β-lactamases in Enterobacteriaceae. Journal of Antimicrobial Chemotherapy, 65(3), 490–495.
De Paula, A. C. L., Medeiros, J. D., De Azevedo, A. C., De Assis Chagas, J. M., Da Silva, V. L., & Diniz, C. G. (2018). Antibiotic Resistance Genetic Markers and Integrons in White Soft Cheese: Aspects of Clinical Resistome and Potentiality of Horizontal Gene Transfer. Genes, 9(2), 106. https://doi.org/10.3390/genes9020106
De Paula Gollino, G., Machado Escobar, B., Dias da Silveira, I., Robales Siqueira, R. H., Ferreira, J. C., Da Costa Darini, A. L., & Bley Ribeiro, V. (2021). Molecular epidemiology of carbapenem-resistant Acinetobacter baumannii from Southern Brazil. Revista de Epidemiologia e Controle de Infecção, 11(1). https://doi.org/10.17058/reci.v1i1.15017
Deng, Y., Bao, X., Ji, L., Chen, L., Liu, J., Miao, J., Chen, D., Bian, H., Li, Y., & Yu, G. (2015). Resistance integrons: Class 1, 2 and 3 integrons. Annals of Clinical Microbiology and Antimicrobials, 14(1), 45. https://doi.org/10.1186/s12941-015-0100-6
Didelot, X., Bowden, R., Wilson, D. J., Peto, T. E., & Crook, D. W. (2012). Transforming clinical microbiology with bacterial genome sequencing. Nature Reviews Genetics, 13(9), 601–612.
El Salabi, A., Walsh, T. R., & Chouchani, C. (2013). Extended spectrum β-lactamases, carbapenemases and mobile genetic elements responsible for antibiotics resistance in Gram-negative bacteria. Critical Reviews in Microbiology, 39(2), 113–122. https://doi.org/10.3109/1040841X.2012.691870
Elkenany, R., Eltaysh, R., Elsayed, M., Abdel-Daim, M., & Shata, R. (2022). Characterization of multi-resistant Shigella species isolated from raw cow milk and milk products. Journal of Veterinary Medical Science, 84(7), 890–897. https://doi.org/10.1292/jvms.22-0018
European Committee on Antimicrobial Susceptibility Testing. (2022). Breakpoint tables for interpretation of MICs and zone diameters. Version 12.0. http://www.eucast.org.
Ghaly, T. M., Chow, L., Asher, A. J., Waldron, L. S., & Gillings, M. R. (2017). Evolution of class 1 integrons: Mobilization and dispersal via food-borne bacteria. PLOS ONE, 12(6), e0179169. https://doi.org/10.1371/journal.pone.0179169
Guo, L., Long, M., Huang, Y., Wu, G., Deng, W., Yang, X., Li, B., Meng, Y., Cheng, L., & Fan, L. (2015). Antimicrobial and disinfectant resistance of E scherichia coli isolated from giant pandas. Journal of Applied Microbiology, 119(1), 55–64.
Hammad, A. M., Eltahan, A., Hassan, H. A., Abbas, N. H., Hussien, H., & Shimamoto, T. (2022). Loads of Coliforms and Fecal Coliforms and Characterization of Thermotolerant Escherichia coli in Fresh Raw Milk Cheese. Foods, 11(3), 332. https://doi.org/10.3390/foods11030332
Hayashi, W., Tanaka, H., Taniguchi, Y., & ... (2019). Acquisition of mcr-1 and Cocarriage of Virulence Genes in Avian Pathogenic Escherichia coli Isolates from Municipal Wastewater Influents in Japan. Applied and …, Query date: 2021-09-17 12:37:32. https://doi.org/10.1128/AEM.01661-19
HiMedia, S. (2011). Agar (Salmonella Shigella Agar).
Hleba, L., Petrová, J., Kántor, A., Čuboň, J., & Kačániová, M. (2015). Antibiotic resistance in Enterobacteriaceae strains isolated from chicken and milk samples. Journal of Microbiology, Biotechnology and Food Sciences, 2015, 19–22.
Kaye, K. S., & Pogue, J. M. (2015). Infections Caused by Resistant Gram-Negative Bacteria: Epidemiology and Management. Pharmacotherapy: The Journal of Human Pharmacology and Drug Therapy, 35(10), 949–962. https://doi.org/10.1002/phar.1636
Koch, B. J., Hungate, B. A., & Price, L. B. (2017). Food-animal production and the spread of antibiotic resistance: The role of ecology. Frontiers in Ecology and the Environment, 15(6), 309–318. https://doi.org/10.1002/fee.1505
Kürekci, C., Arkadaş, M., & Avşar, Y. K. (2016). Occurrence, genetic characterization and antimicrobial resistance of extended spectrum β-lactamase producing Escherichia coli isolated from Sürk samples, a traditional turkish cheese. Journal of Food Measurement and Characterization, 10(3), 709–714. https://doi.org/10.1007/s11694-016-9355-7
Lanz, R., Kuhnert, P., & Boerlin, P. (2003). Antimicrobial resistance and resistance gene determinants in clinical Escherichia coli from different animal species in Switzerland. Veterinary microbiology, 91(1), 73–84.
Leflon-Guibout, V., Jurand, C., Bonacorsi, S., Espinasse, F., Guelfi, M. C., Duportail, F., Heym, B., Bingen, E., & Nicolas-Chanoine, M.-H. (2004). Emergence and spread of three clonally related virulent isolates of CTX-M-15-producing Escherichia coli with variable resistance to aminoglycosides and tetracycline in a French geriatric hospital. Antimicrobial Agents and Chemotherapy, 48(10), 3736–3742.
Lund, B. M., & O’Brien, S. J. (2011). The Occurrence and Prevention of Foodborne Disease in Vulnerable People. Foodborne Pathogens and Disease, 8(9), 961–973. https://doi.org/10.1089/fpd.2011.0860
Martins, A. F., & Rabinowitz, P. (2020). The impact of antimicrobial resistance in the environment on public health. Future Microbiology, 15(9), 699–702. https://doi.org/10.2217/fmb-2019-0331
Nagy, Á., Székelyhidi, R., Hanczné Lakatos, E., & Kapcsándi, V. (2021). Review on the occurrence of the mcr-1 gene causing colistin resistance in cow’s milk and dairy products. Heliyon, 7(4), e06800. https://doi.org/10.1016/j.heliyon.2021.e06800
Nielsen, K. M., Domingues, S., & da Silva, G. J. (2015). Global dissemination patterns of common gene cassette arrays in class 1 integrons. Microbiology, 161(7), 1313–1337. https://doi.org/10.1099/mic.0.000099
Nilsson, V. (2021). The occurrence of antibiotic resistant bacteria in Swedish dairy products–A pilot study.
Nisha, A. (2008). Antibiotic residues-a global health hazard. Veterinary world, 1(12), 375.
O’Neill, J. (2014). Review on antimicrobial resistance. Antimicrobial resistance: tackling a crisis for the health and wealth of nations, 2014(4).
Organização Pan-Americana da Saúde. (2020). Resistência antimicrobiana—OPAS/OMS. https://www.paho.org/pt/topicos/resistencia-antimicrobiana.
Paterson, D. L., & Bonomo, R. A. (2005). Extended-Spectrum β-Lactamases: A Clinical Update. Clinical Microbiology Reviews, 18(4), 657–686. https://doi.org/10.1128/CMR.18.4.657-686.2005
Peirano, G., Agersø, Y., Aarestrup, F. M., dos Reis, E. M. F., & dos Prazeres Rodrigues, D. (2006). Occurrence of integrons and antimicrobial resistance genes among Salmonella enterica from Brazil. Journal of Antimicrobial Chemotherapy, 58(2), 305–309. https://doi.org/10.1093/jac/dkl248
Poirel, L., Walsh, T. R., Cuvillier, V., & Nordmann, P. (2011). Multiplex PCR for detection of acquired carbapenemase genes. Diagnostic microbiology and infectious disease, 70(1), 119–123.
Quintieri, Fanelli, & Caputo. (2019). Antibiotic Resistant Pseudomonas Spp. Spoilers in Fresh Dairy Products: An Underestimated Risk and the Control Strategies. Foods, 8(9), 372. https://doi.org/10.3390/foods8090372
Randall, C. P., Mariner, K. R., Chopra, I., & O’Neill, A. J. (2013). The target of daptomycin is absent from Escherichia coli and other gram-negative pathogens. Antimicrobial agents and chemotherapy, 57(1), 637–639.
San Millan, A. (2018). Evolution of plasmid-mediated antibiotic resistance in the clinical context. Trends in microbiology, 26(12), 978–985.
Silva, C. R., Okuno, N. T., Macedo, V. H. L. de M., Freire, I. D. R., Miller, R. M., & Marin, V. A. (2020). Resistome in gram-negative bacteria from soft cheese in Brazil. Revista de Ciências Médicas e Biológicas, 19(3), 430. https://doi.org/10.9771/cmbio.v19i3.35460
Tabaran, A., Soulageon, V., Chirila, F., Reget, O. L., Mihaiu, M., Borzan, M., & Dan, S. D. (2022). Pathogenic E. coli from Cattle as a Reservoir of Resistance Genes to Various Groups of Antibiotics. Antibiotics, 11(3), 404. https://doi.org/10.3390/antibiotics11030404
Trocado, N. D., de Moraes, M. S., Aveleda, L., Silva, C. R., & Marin, V. A. (2021). Phenotypic and genotypic detection of antibiotic-resistant bacteria in fresh fruit juices from a public hospital in Rio de Janeiro. Archives of Microbiology, 203(4), 1471–1475. https://doi.org/10.1007/s00203-020-02139-9
Uyanik, T., Çadirci, Ö., Gücükoğlu, A., & Can, C. (2022). Investigation of major carbapenemase genes in ESBL-producing Escherichia coli and Klebsiella pneumoniae strains isolated from raw milk in Black Sea region of Turkey. International Dairy Journal, 128, 105315. https://doi.org/10.1016/j.idairyj.2021.105315
World Health Organization. (2017). WHO publishes list of bacteria for which new antibiotics are urgently needed. https://www.who.int/news/item/27-02-2017-who-publishes-list-of-bacteria-for-which-new-antibiotics-are-urgently-needed
World Health Organization. (2020). Antibiotic resistance. https://www.who.int/news-room/fact-sheets/detail/antibiotic-resistance
Xiong, L., Sun, Y., Shi, L., & Yan, H. (2019). Characterization of antimicrobial resistance genes and class 1 integrase gene in raw meat and aquatic product, fresh vegetable and fruit, and swine manure in southern China. Food Control, 104, 240–246. https://doi.org/10.1016/j.foodcont.2019.05.004KUR
Xu, G., An, W., Wang, H., & Zhang, X. (2015). Prevalence and characteristics of extended-spectrum β-lactamase genes in Escherichia coli isolated from piglets with post-weaning diarrhea in Heilongjiang province, China. Frontiers in Microbiology, 6. https://doi.org/10.3389/fmicb.2015.01103
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Copyright (c) 2022 Fabiana Montovanele de Melo; Cristiane Rodrigues Silva; Gabriel Lopes Carvalho; Victor Augustus Marin
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