Efficacy of Caryocar brasiliense Camb. and Annona crassiflora Mart. leaves in the reduction of biotransferred Escherichia coli from Lactuca sativa L. leaves to polypropylene
Keywords:Bacterial adhesion; Biofilms; Cross contamination; Sanitization.
The antimicrobial activity of Caryocar brasiliense and Annona crassiflora leaves extracts was evaluated against Escherichia coli strains through a sensitivity test by the agar diffusion method and by the evaluation of minimal inhibitory concentrations (MIC) and minimal bactericidal concentrations (MBC) by the microdilution technique followed by plating. The sanitizing efficiency of these extracts in reducing E. coli cells biotransferred from L. sativa leaves to polypropylene surfaces was evaluated after an exposure time of 5 minutes. All strains were sensitive to antibacterials and the formation of an inhibition halo was observed for the extracts against all strains tested. The C. brasiliense extract showed better antimicrobial action against E. coli strains, with a MIC of 1.09 mg/mL, while the MIC of A. crassiflora extract was 5.58 mg/mL. No MBC was found for plant extracts. The strains were not able to form biofilms under the conditions studied, however, there was biotransfer and adhesion of E. coli to polypropylene. The highest counts of E. coli cells biotransferred and, consequently, adhere to the polypropylene coupons were observed when 5 log CFU/mL was inoculated, with a mean count of 4.53 ± 0.66 log CFU/cm2. It was verified that the treatment with the extract solutions in the minimum inhibitory concentrations (MIC) totally reduced the number of E. coli cells adhered to the polypropylene coupons. The results obtained indicate that the use of extracts from both species as antibacterials is promising.
Adamczak, A. (2020). Antibacterial Activity of Some Flavonoids and Organic Acids Widely Distributed in Plants. Journal of Clinical Medicine, 109(9), 1–17.
Alvares, C. A., Stape, J. L., Sentelhas, P. C., Gonçalves, J. L. de M., & Sparovek, G. (2014). Koppen’s climate classification map for Brazil. Meteorologische Zeitschrift, 22(6), 711–728. https://doi.org/10.1127/0941-2948/2013/0507
Andrade, N. J., Bridgeman, T. A., & Zottola, E. A. (1998). Bacteriocidal Activity of Sanitizers against Enterococcus faecium Attached to Stainless Steel as Determined by Plate Count and Impedance Methods. Journal of Food Protection, 61(7), 833–838.
Calo, J. R., Crandall, P. G., O’Bryan, C. A., & Ricke, S. C. (2015). Essential oils as antimicrobials in food systems - A review. Food Control, 54, 111–119. https://doi.org/10.1016/j.foodcont.2014.12.040
Careli, R. T., Andrade, N. J., Soares, N. F., Júnior, J. I. R., Rosado, M. S., & Bernardes, P. C. (2009). The adherence of Pseudomonas fluorescens to marble , granite , synthetic polymers , and stainless steel. Ciência e Tecnologia de Alimentos, 29(1), 171–176.
Carlie, S. M., Boucher, C. E., & Bragg, R. R. (2020). Molecular basis of bacterial disinfectant resistance. Drug Resistance Updates, 48, 1–9. https://doi.org/10.1016/j.drup.2019.100672
Ceuppens, S., Titze, C., Quadros, R. De, Bartz, S., César, E., & Uyttendaele, M. (2014). Microbiological quality and safety assessment of lettuce production in Brazil. International Journal of Food Microbiology, 181, 67–76. https://doi.org/10.1016/j.ijfoodmicro.2014.04.025
Cunnif, P. (1995). Official methods of AOAC International (16th ed.). AOAC International.
Del-claro, K., & Torezan-silingardi, H. M. (2019). The study of biotic interactions in the Brazilian Cerrado as a path to the conservation of biodiversity. Annals of the Brazilian Academy of Sciences, 91(3), 1–6. https://doi.org/10.1590/0001-3765201920180768
Djipa, C. D., Delme, M., & Quetin-Leclercq, J. (2000). Antimicrobial activity of bark extracts of Syzygium jambos (L.) Alston (Myrtaceae). Journal of Ethnopharmacology, 71, 307–313.
Dušková, M., Šedo, O., Kšicová, K., Zdráhal, Z., & Karpíšková, R. (2012). Identification of lactobacilli isolated from food by genotypic methods and MALDI-TOF MS. International Journal of Food Microbiology, 159, 107–114. https://doi.org/10.1016/j.ijfoodmicro.2012.07.029
Feltes, M. M. C., Arisseto-Bragotto, A. P., & Block, J. M. (2017). Food quality, food-borne diseases, and food safety in the Brazilian food industry. Food Quality and Safety, 1(1), 13–27. https://doi.org/10.1093/fqs/fyx003
Flemming, H., Wingender, J., Szewzyk, U., Steinberg, P., & Rice, S. A. (2016). Biofilms : an emergent form of bacterial life. Nature Reviews, 14(9), 563–575. https://doi.org/10.1038/nrmicro.2016.94
Franco, F. D., Tranchida, G., Pupillo, D., Ghersi, G., Cin, P., Virtanen, S., & Santamaria, M. (2021). Effect of E. coli Biofilm formation and removal on passive films on AISI 316L during fermentation processes. Corrosion Science, 1–31. https://doi.org/10.1016/j.corsci.2021.109430
Freiwald, A., & Sauer, S. (2009). Phylogenetic classification and identification of bacteria by mass spectrometry. Nature Protocols, 4(5), 732–742. https://doi.org/10.1038/nprot.2009.37
Galié, S., García-gutiérrez, C., Miguélez, E. M., Villar, C. J., Lombó, F., & Bonaventura, G. Di. (2018). Biofilms in the Food Industry : Health Aspects and Control Methods. Frontiers in Microbiology, 9, 1–18. https://doi.org/10.3389/fmicb.2018.00898
Gonelimali, F. D., Lin, J., Miao, W., Xuan, J., Charles, F., Chen, M., & Hatab, S. R. (2018). Antimicrobial Properties and Mechanism of Action of Some Plant Extracts Against Food Pathogens and Spoilage Microorganisms. Frontiers in Microbiology, 9, 1–9. https://doi.org/10.3389/fmicb.2018.01639
Górniak, I., Bartoszewski, R., & Króliczewski, J. (2018). Comprehensive review of antimicrobial activities of plant flavonoids. Phytochem Rev., 18, 241–272. https://doi.org/10.1007/s11101-018-9591-z
Kannan, M., Rajarathinam, K., Venkatesan, S., Dheeba, B., & Maniraj, A. (2017). Silver Iodide nanoparticles as an antibiofilm agent - A case study on gram-negative biofilm-forming bacteria. In A. Ficai & A. M. Grumezescu (Eds.), Nanostructures for Antimicrobial Therapy (1st ed., pp. 435–456). Elsevier. https://doi.org/10.1016/B978-0-323-46152-8.00019-6
Klančnik, A., Piskernik, S., Jeršek, B., & Možina, S. S. (2010). Evaluation of diffusion and dilution methods to determine the antibacterial activity of plant extracts. Journal of Microbiological Methods, 81, 121–126. https://doi.org/10.1016/j.mimet.2010.02.004
Koo, O., Martin, E. M., Story, R., Lindsay, D., Ricke, S. C., & Crandall, P. G. (2013). Comparison of cleaning fabrics for bacterial removal from food-contact surfaces. Food Control, 30(1), 292–297. https://doi.org/10.1016/j.foodcont.2012.06.008
Kornacki, J. L., & Johnson, J. L. (2001). Enterobacteriaceae, coliforms, and Escherichia coli as quality and safety indicators. In F. P. Downes & K. Ito (Eds.), Compendium of Methods for the Microbiological Examination of Foods (4th ed., pp. 69–82). APHA.
Kregiel, D. (2014). Advances in biofilm control for food and beverage industry using organo-silane technology : A review. Food Control, 40, 32–40. https://doi.org/10.1016/j.foodcont.2013.11.014
Lima, P. M., São, J. F. B., Andrade, N. J., Clarissa, A., Pires, S., & Ferreira, S. O. (2013). Interaction between natural microbiota and physicochemical characteristics of lettuce surfaces can influence the attachment of Salmonella Enteritidis. Food Control, 30(1), 157–161. https://doi.org/10.1016/j.foodcont.2012.06.039
Lopes, T. da C., Gonçalves, J. de R. S., Souza, N. S., Moraes, D. F. C., Amaral, F. M. M. do, & Rosa, I. G. (2011). Avaliação moluscicida e perfil fitoquímico das folhas de Caryocar brasiliense Camb. Cadernos de Pesquisa, 18(3), 23–30.
Luna-Guevara, J. J., Arenas-Hernandez, M. M. P., Peña, C. M. de la, Silva, J. L., & Luna-Guevara, M. L. (2019). The Role of Pathogenic E. coli in Fresh Vegetables: Behavior, Contamination Factors, and Preventive Measures. International, 2019, 1–10.
Machado, A. R. T., Ferreira, S. R., Medeiros, F. da S., Fujiwara, R. T., Filho, J. D. de S., Santos, L. P., & Pimenta. (2015). Nematicidal activity of Annona crassiflora leaf extract on Caenorhabditis elegans. Parasites & Vectors, 8, 1–5. https://doi.org/10.1186/s13071-015-0708-6
Malheiros, S., Tavares, C., Casarin, L. S., Serraglio, L., & Tondo, E. C. (2010). Evaluation of growth and transfer of Staphylococcus aureus from poultry meat to surfaces of stainless steel and polyethylene and their disinfection. Food Control, 21(3), 298–301. https://doi.org/10.1016/j.foodcont.2009.06.008
Morais-costa, F., Bastos, G. A., Soares, A. C. M., Costa, E. G. L., Vasconcelos, V. O., Oliveira, N. J. F., Braga, F. C., Duarte, E. R., & Lima, W. S. (2016). Veterinary Parasitology In vitro and in vivo action of Piptadenia viridiflora ( Kunth ) Benth against Haemonchus contortus in sheep. Veterinary Parasitology, 223, 43–49. https://doi.org/10.1016/j.vetpar.2016.04.002
Morais, H. L. M. do N., Feitosa, T. C., Rodrigues, J. G. M., Lira, M. G. S., Nogueira, R. A., Luz, T. R. S. A., Silva-Souza, N., Lima, N. M., Andrade, T. de J. A. dos S., & Miranda, G. S. (2020). Hydroalcoholic extract of Caryocar brasiliense Cambess . leaves affect the development of Aedes aegypti mosquitoes. Journal of the Brazilian Society of Tropical Medicine, 53, 1–7.
Nahar, S., Ha, A. J., Byun, K., & Hossain, I. (2021). Efficacy of flavourzyme against Salmonella Typhimurium , Escherichia coli, and Pseudomonas aeruginosa biofilms on food-contact surfaces. International Journal of Food Microbiology, 336, 1–11. https://doi.org/10.1016/j.ijfoodmicro.2020.108897
Oliveira, C. da C., Matos, N. A. de, Veloso, C. de C., Lage, G. A., Santos, L. P., Pimenta, Duarte, I. D. G., Romero, T. R. L., Klein, A., & Perez, A. de C. (2018). Anti-inflammatory and antinociceptive properties of the hydroalcoholic fractions from the leaves of Annona crassiflora Mart . in mice. Inflammopharmacology, 27, 397–408. https://doi.org/10.1007/s10787-017-0426-0
Paula-Junior, W. de, Rocha, F. H., Donatti, L., Fadel-Picheth, C. M. T., & Weffort-Santos, A. M. (2006). Leishmanicidal, antibacterial, and antioxidant activities of Caryocar brasiliense Cambess leaves hydroethanolic extract. Brazilian Journal of Pharmacognosy, 16, 625–630.
Pinho, L. de, Souza, P. N. S., Sobrinho, E. M., Almeida, A. C. de, & Martins, E. R. (2012). Atividade antimicrobiana de extratos hidroalcoolicos das folhas de alecrim- pimenta, aroeira, barbatimão, erva baleeira e do farelo da casca de pequi. Ciência Rural, 42(2), 326–331.
Ribeiro, I. C. D. O., Mariano, E. G. A., Careli, R. T., Morais-costa, F., Anna, F. M. D. S., Pinto, M. S., Souza, M. R. De, & Duarte, E. R. (2018). Plants of the Cerrado with antimicrobial effects against Staphylococcus spp . and Escherichia coli from cattle. BMC Veterinary Research, 14, 1–10. https://doi.org/10.1186/s12917-018-1351-1
Rocha, C. R., Careli, R. T., Silva, R. P., Almeida, A. C. de, Martins, E. R., Oliveira, E. M. B., & Duarte, E. R. (2014). Óleo essencial de Rosmarinus officinalis L. como sanitizante natural para controle de bactérias sésseis em superfície utilizada para corte de alimentos. Rev Inst Adolfo Lutz, 73(4), 338–344. https://doi.org/10.18241/0073-98552014731624
Rossoni, E. M. M., & Gaylarde, C. C. (2000). Comparison of sodium hypochlorite and peracetic acid as sanitising agents for stainless steel food processing surfaces using epifluorescence microscopy. International Journal of Food Microbiology, 61, 81–85.
Sanchez-Vizuete, P., Orgaz, B., Aymerich, S., Coq, D. Le, & Briandet, R. (2015). Pathogens protection against the action of disinfectants in multispecies biofilms. Frontiers in Microbiology, 6, 1–12. https://doi.org/10.3389/fmicb.2015.00705
Vidács, A., Kerekes, E., Rajkó, R., Petkovits, T., Alharbi, N. S., Khaled, J. M., Vágvölgyi, C., & Krisch, J. (2018). Optimization of essential oil-based natural disinfectants against Listeria monocytogenes and Escherichia coli biofilms formed on polypropylene surfaces. Journal of Molecular Liquids, 255, 257–262. https://doi.org/10.1016/j.molliq.2018.01.179
Wang, Y., Liang, Z., Liao, X., Zhou, C., Xie, Z., Zhu, S., & Wei, G. (2019). Identification of C‑glycosyl flavones by high performance liquid chromatography electrospray ionization mass spectrometry and quantification of five main C‑glycosyl flavones in Flickingeria fimbriata. BMC Chemistry, 13(94), 1–20. https://doi.org/10.1186/s13065-019-0616-5
Weerarathne, P., Payne, J., Saha, J., Kountoupis, T., Jadeja, R., & Jaroni, D. (2021). Evaluating the efficacy of sodium acid sulfate to reduce Escherichia coli O157 : H7 and its biofilms on food-contact surfaces. LWT - Food Science and Technology, 139, 1–7. https://doi.org/10.1016/j.lwt.2020.110501
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Copyright (c) 2021 Larissa Lorrane Rodrigues Borges; Alécia Daila Barros Guimarães; Fanciellen Morais-Costa; Eduardo Robson Duarte; Márcia Martins; Roberta Torres Careli
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