Effect of gaseous ozone treatment on biofilm of dairy-isolated Pseudomonas spp. strains
https://doi.org/10.4081/ijfs.2022.10350
Accepted: 24 February 2022
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Microbial biofilms existing in food industries have been implicated as important contamination sources of spoilage and pathogenic microorganisms in the finished products. Among the innovative strategies proposed to contrast biofilms in food environments, ozone is recognised as an environmentally friendly technology but there are few studies about its effect against bacterial biofilms. The objective of this study was to evaluate the effect of gaseous ozone (50 ppm for 6 h) in inhibition and eradication of biofilm formed by twenty-one dairyisolated Pseudomonas spp. strains. Before ozone treatments, all isolates were screened for biofilm formation according to a previously described method. Strains were then divided in four groups: weak, weak/moderate, moderate/strong, and strong biofilm producers based on the biofilm biomass value of each isolate determined using the optical density (OD - 595 nm). Inhibition treatment was effective on the strain (C1) belonging to the weak producers’ group, on all strains classified as weak/moderate producers, on two strains (C8 and C12) belonging to the group of moderate/strong producers and on one strain (C13) classified as strong producer. Conversely, eradication treatments were ineffective on all strains tested, except for the strain C4 which reduced its biofilm-forming abilities after exposure to ozone gas. In conclusion, gaseous ozone may be used to enhance existing sanitation protocols in food processing environments, but its application alone not seems sufficient to contrast Pseudomonas spp. established biofilms.
Aponte M, Anastasio A, Marrone R, Mercogliano R, Peruzy MF, Murru N, 2018. Impact of gaseous ozone coupled to passive refrigeration system to maximize shelf-life and quality of four different fresh fish products. LWT 93:412–9. DOI: https://doi.org/10.1016/j.lwt.2018.03.073
Baumann AR, Martin SE, Feng H, 2009. Removal of Listeria monocytogenes biofilms from stainless steel by use of ultrasound and ozone. J Food Prot 72:1306-9. DOI: https://doi.org/10.4315/0362-028X-72.6.1306
Bialka KL, Demirci A. 2007. Decontamination of Escherichia coli O157:H7 and Salmonella enterica on blueberries using ozone and pulsed UV-light. J Food Sci 72:M391–6. DOI: https://doi.org/10.1111/j.1750-3841.2007.00517.x
Bigi F, Haghighi H, Quartieri A, Leo RD, Pulvirenti A. 2021. Impact of low-dose gaseous ozone treatment to reduce the growth of in vitro broth cultures of foodborne pathogenic/spoilage bacteria in a food storage cold chamber. J Food Saf 41:e12892. DOI: https://doi.org/10.1111/jfs.12892
Botondi R, Barone M, Grasso C, 2021. A review into the effectiveness of ozone technology for improving the safety and preserving the quality of fresh-cut fruits and vegetables. Foods 10:748. DOI: https://doi.org/10.3390/foods10040748
Botta C, Ferrocino I, Pessione A, Cocolin L, Rantsiou K. Spatiotemporal distribution of the environmental microbiota in food processing plants as impacted by cleaning and sanitizing procedures: the case of slaughterhouses and gaseous ozone. Appl Environ Microbiol 86:e01861-20. DOI: https://doi.org/10.1128/AEM.01861-20
Brodowska AJ, Nowak A, Śmigielski K. 2018. Ozone in the food industry: Principles of ozone treatment, mechanisms of action, and applications: An overview. Crit Rev Food Sci Nutr 58:2176-201. DOI: https://doi.org/10.1080/10408398.2017.1308313
Carrascosa C, Raheem D, Ramos F, Saraiva A, Raposo A, 2021. Microbial biofilms in the food industry - a comprehensive review. Int J Environ Res Public Health 18:2014. DOI: https://doi.org/10.3390/ijerph18042014
Cenci-Goga BT, Karama M, Sechi P, Iulietto MF, Novelli S, Mattei S, 2014. Evolution under different storage conditions of anomalous blue coloration of Mozzarella cheese intentionally contaminated with a pigment-producing strain of Pseudomonas fluorescens. J Dairy Sci 97:6708-18. DOI: https://doi.org/10.3168/jds.2014-8611
Chmielewski R a. N, Frank JF. 2003. Biofilm formation and control in food processing facilities. Compr Rev Food Sci Food Saf 2:22-32. DOI: https://doi.org/10.1111/j.1541-4337.2003.tb00012.x
Cleto S, Matos S, Kluskens L, Vieira MJ. 2012. Characterization of contaminants from a sanitized milk processing plant. PLoS One 7:e40189. DOI: https://doi.org/10.1371/journal.pone.0040189
De Jonghe V, Coorevits A, Van Hoorde K, Messens W, Van Landschoot A, De Vos P, Heyndrickx M. 2011. Influence of storage conditions on the growth of Pseudomonas species in refrigerated raw milk. Appl Environ Microbiol 77:460-70. DOI: https://doi.org/10.1128/AEM.00521-10
Eneroth Å, Ahrné S, Molin G, 2000. Contamination of milk with Gram-negative spoilage bacteria during filling of retail containers. Int J Food Microbiol 57:99–106. DOI: https://doi.org/10.1016/S0168-1605(00)00239-7
Frank JF, 2001. Microbial attachment to food and food contact surfaces. In Advances in Food and Nutrition Research. pp. 319–370. Elsevier. DOI: https://doi.org/10.1016/S1043-4526(01)43008-7
González-Rivas F, Ripolles-Avila C, Fontecha-Umaña F, Ríos-Castillo AG, Rodríguez-Jerez JJ. 2018. Biofilms in the spotlight: detection, quantification, and removal methods. Compr Rev Food Sci Food Saf 17:1261-76. DOI: https://doi.org/10.1111/1541-4337.12378
Guzzon R, Franciosi E, Carafa I, Larcher R, Tuohy K. 2015. The ozone, an innovative tool for microbiological control in dairies. Industrie Alimentari 53:11-5.
Irie Y, Starkey M, Edwards AN, Wozniak DJ, Romeo T, Parsek MR, 2010. Pseudomonas aeruginosa biofilm matrix polysaccharide Psl is regulated transcriptionally by RpoS and post-transcriptionally by RsmA. Mol Microbiol 78:158–72. DOI: https://doi.org/10.1111/j.1365-2958.2010.07320.x
Italian Ministry of Health. 2010. [Opinion of the National Food Safety Committee on ozone treatment of air in cheese ripening rooms]. Retrieved from http://www.salute.gov.it/imgs/C_17_pubblicazioni_1514_allegato.pdf [In Italian]
Kim JG, Yousef AE, Dave S, 1999. Application of ozone for enhancing the microbiological safety and quality of foods: A Review. J Food Prot 62:1071–1087. DOI: https://doi.org/10.4315/0362-028X-62.9.1071
Kives J, Orgaz B, SanJosé C, 2006. Polysaccharide differences between planktonic and biofilm-associated EPS from Pseudomonas fluorescens B52. Colloids Surf B Biointerfaces 52:123–127. DOI: https://doi.org/10.1016/j.colsurfb.2006.04.018
Marino M, Maifreni M, Baggio A, Innocente N, 2018. Inactivation of foodborne bacteria biofilms by aqueous and gaseous ozone. Front Microbiol 9:2024. DOI: https://doi.org/10.3389/fmicb.2018.02024
Muhammad MH, Idris AL, Fan X, Guo Y, Yu Y, Jin X, Qiu J, Guan X, Huang T, 2020. Beyond risk: bacterial biofilms and their regulating approaches. Front Microbiol 11:928. DOI: https://doi.org/10.3389/fmicb.2020.00928
Panebianco F, Rubiola S, Di Ciccio PA, 2022. The Use of Ozone as an Eco-Friendly Strategy against Microbial Biofilm in Dairy Manufacturing Plants: A Review. Microorganisms 10:162. DOI: https://doi.org/10.3390/microorganisms10010162
Panebianco F, Rubiola S, Chiesa F, Civera T, Di Ciccio PA, 2021. Effect of gaseous ozone on Listeria monocytogenes planktonic cells and biofilm: an in vitro study. Foods 10:1484. DOI: https://doi.org/10.3390/foods10071484
Reichler SJ, Trmčić A, Martin NH, Boor KJ, Wiedmann M, 2018. Pseudomonas fluorescens group bacterial strains are responsible for repeat and sporadic postpasteurization contamination and reduced fluid milk shelf life. J Dairy Sci 101:7780–800. DOI: https://doi.org/10.3168/jds.2018-14438
Rossi C, Chaves-López C, Serio A, Goffredo E, Goga BTC, Paparella A, 2016. Influence of incubation conditions on biofilm formation by Pseudomonas fluorescens isolated from dairy products and dairy manufacturing plants. Ital J Food Saf 5:5793. DOI: https://doi.org/10.4081/ijfs.2016.5793
Rossi C, Serio A, Chaves-López C, Anniballi F, Auricchio B, Goffredo E, Cenci-Goga BT, Lista F, Fillo S, Paparella A, 2018. Biofilm formation, pigment production and motility in Pseudomonas spp. isolated from the dairy industry. Food Control 86:241–8. DOI: https://doi.org/10.1016/j.foodcont.2017.11.018
Segat A, Biasutti M, Iacumin L, Comi G, Baruzzi F, Carboni C, Innocente N. 2014. Use of ozone in production chain of high moisture Mozzarella cheese. LWT - Food Sci Technol 55:513–20. DOI: https://doi.org/10.1016/j.lwt.2013.10.029
Sheng L, Hanrahan I, Sun X, Taylor MH, Mendoza M, Zhu MJ, 2018. Survival of Listeria innocua on Fuji apples under commercial cold storage with or without low dose continuous ozone gaseous. Food Microbiol 76:21-8. DOI: https://doi.org/10.1016/j.fm.2018.04.006
Sofos JN, Geornaras I. 2010. Overview of current meat hygiene and safety risks and summary of recent studies on biofilms, and control of Escherichia coli O157:H7 in nonintact, and Listeria monocytogenes in ready-to-eat, meat products. Meat Sci 86:2–14. DOI: https://doi.org/10.1016/j.meatsci.2010.04.015
Stepanović S, Vuković D, Hola V, Bonaventura GD, Djukić S, Ćirković I, Ruzicka F, 2007. Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS 115:891-9. DOI: https://doi.org/10.1111/j.1600-0463.2007.apm_630.x
Teh KH, Flint S, Palmer J, Andrewes P, Bremer P, Lindsay D. 2014. Biofilm - An unrecognised source of spoilage enzymes in dairy products? Int Dairy J 34:32-40. DOI: https://doi.org/10.1016/j.idairyj.2013.07.002
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