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Ozonation for Pseudomonas paracarnis control: biofilm removal and preservation of chicken meat during refrigerated storage

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Abstract

Ozone has been studied to control microorganisms in food, as well as to control biofilm. In this context, the goals of this work were to determine the effect of ozonated water in the removal of Pseudomonas paracarnis biofilm and the effect of ozone gas and ozonated water on inactivating P. paracarnis in deboned chicken breast meat and its effect on product color. AISI 304 coupons were used as a surface for biofilm formation. The coupons were immerged into minimal medium for Pseudomonas inoculated with the P. paracarnis overnight culture (1% w/v) followed by incubation at 25 °C for 7 days. To obtain ozonized water, two different systems were used: system with microbubble generator (MB) and system with porous stone diffuser (PSD). The inlet ozone concentration was 19 mg/L and flow rate of 1 L/min. The coupons were subjected to ozonized water for 10 and 20 min. The chicken breast meat was exposed to gaseous ozone and ozonized water for 40 min. After the ozonation process, chicken meat samples were stored at 8 °C, for 5 days. More expressive removals of biofilm were obtained when using ozonized water obtained in the system with microbubble generator (MB for 20 min—reduction of 2.3 log cycles) and system with porous stone diffuser (PSD for 10 min—reduction of 2.7 log cycles; PSD for 20 min—reduction of 2.6 log cycles). The treatment of chicken meat with ozone gas resulted in lower counting of Pseudomonas, when compared with the control treatments and with ozonized water, both immediately after ozonation (day 1) and after 5 days of storage. The luminosity in the chicken meat samples treated with ozonized water was higher than that verified in the control treatments and with ozone gas, immediately after ozonation (day 1). A similar trend was observed in hue angle and color difference, in which the highest values were obtained for treatment with ozonized water. Based on the results obtained in this study, it was concluded that ozonated water can be used to remove P. paracarnis biofilm from stainless steel under static conditions and gaseous ozone is more efficient in the inactivation of P. paracarnis from chicken breast meat, when compared to ozonated water.

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References

  1. Samapundo S, de Baenst I, Aerts M, Cnockaert M, Devlieghere F, Van Damme P (2019) Tracking the sources of psychrotrophic bacteria contaminating chicken cuts during processing. Food Microbiol 81:40–50. https://doi.org/10.1016/j.fm.2018.06.003

    Article  CAS  PubMed  Google Scholar 

  2. Ayranci UG, Ozunlu O, Ergezer H, Karaca H (2020) Effects of ozone treatment on microbiological quality and physicochemical properties of turkey breast meat. Ozone-Sci Eng 42(1):95–103. https://doi.org/10.1080/01919512.2019.1653168

    Article  CAS  Google Scholar 

  3. Nel S, Lues JFR, Buys EM, Venter P (2004) Bacterial populations associated with meat from the deboning room of a high throughput red meat abattoir. Meat sci 66(3):667–674. https://doi.org/10.1016/S0309-1740(03)00187-6

    Article  CAS  PubMed  Google Scholar 

  4. Shale K, Jacoby A, Plaatjies Z (2006) The impact of extrinsic sources on selected indicator organisms in a typical deboning room. Int J Environ Health Res 16(4):263–272. https://doi.org/10.1080/09603120600734162

    Article  PubMed  Google Scholar 

  5. Williams GD, Keener KM (2008) Design considerations for the construction and operation of meat and poultry processing facilities. In: Proc Annu Int Meet Am Soc Agric Biol Eng 2008. Providence, pp 1–25. https://doi.org/10.13031/2013.24882

  6. Botta C, Ferrocino I, Pessione A, Cocolin L, Rantsiou K (2020) 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(23):e01861-e1920. https://doi.org/10.1128/AEM.01861-20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Chen SH, Fegan N, Kocharunchitt C, Bowman JP, Duffy LL (2020) Changes of the bacterial community diversity on chicken carcasses through an Australian poultry processing line. Food Microb 86:103350. https://doi.org/10.1016/j.fm.2019.103350

    Article  CAS  Google Scholar 

  8. Wickramasinghe NN, Ravensdale J, Coorey R, Chandry SP, Dykes GA (2019) The predominance of psychrotrophic pseudomonads on aerobically stored chilled red meat. Compr Rev Food Sci Food Saf 18(5):1622–1635. https://doi.org/10.1111/1541-4337.12483

    Article  CAS  PubMed  Google Scholar 

  9. Rajmohan S, Dodd CER, Waites WM (2002) Enzymes from isolates of Pseudomonas fluorescens involved in food spoilage. J Appl Microbiol 93(2):205–213. https://doi.org/10.1046/j.1365-2672.2002.01674.x

    Article  CAS  PubMed  Google Scholar 

  10. Lick S, Kröckel L, Wibberg D, Winkler A, Blom J, Bantleon A et al (2020) Pseudomonas carnis sp. nov,. isolated from meat. Int J Syst Evol Microbiol 70(3):1528–1540. https://doi.org/10.1099/ijsem.0.003928

    Article  CAS  PubMed  Google Scholar 

  11. Lick S, Wibberg D, Winkler A, Blom J, Grimmler C, Goesmann A et al (2021) Pseudomonas paracarnis sp. nov,. isolated from refrigerated beef. Int J Syst Evol Microbiol 71(2):004652. https://doi.org/10.1099/ijsem.0.004652

    Article  CAS  Google Scholar 

  12. Marino M, Maifreni M, Baggio A, Innocente N (2018) Inactivation of foodborne bacteria biofilms by aqueous and gaseous ozone. Front Microbiol 9:1–12. https://doi.org/10.3389/fmicb.2018.02024

    Article  Google Scholar 

  13. Waters EM, Rowe SE, O’Gara JP, Conlon BP (2016) Convergence of Staphylococcus aureus persister and biofilm research: can biofilms be defined as communities of adherent persister cells? PLoS Pathog 12(12):e1006012. https://doi.org/10.1371/journal.ppat.1006012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Masák J, Čejková A, Schreiberová O, Řezanka T (2014) Pseudomonas biofilms: possibilities of their control. FEMS Microbiol Ecol 89(1):1–14. https://doi.org/10.1111/1574-6941.12344

    Article  CAS  PubMed  Google Scholar 

  15. Kim JG, Yousef AE, Dave S (1999) Application of ozone for enhancing the microbiological safety and quality of foods: a review. J Food Protect 62:1071–1087. https://doi.org/10.4315/0362-028x-62.9.1071

    Article  CAS  Google Scholar 

  16. Cullen PJ, Tiwari BK, O’Donnell CP, Muthukumarappan K (2009) Modelling approaches to ozone processing of liquid foods. Trends Food Sci Technol 20(3–4):125–136. https://doi.org/10.1016/j.tifs.2009.01.049

    Article  CAS  Google Scholar 

  17. Alencar ER, Faroni LRDA, Soares NDFF, da Silva WA, da Silva Carvalho MC (2012) Efficacy of ozone as a fungicidal and detoxifying agent of aflatoxins in peanuts. J Sci Food Agric 92(4):899–905. https://doi.org/10.1002/jsfa.4668

    Article  CAS  PubMed  Google Scholar 

  18. Epelle EI, Macfarlane A, Cusack M, Burns A, Thissera B, Mackay W, Rateb ME (2022) Bacterial and fungal disinfection via ozonation in air. J Microbiol Methods 194:106431. https://doi.org/10.1016/j.mimet.2022.106431

    Article  CAS  PubMed  Google Scholar 

  19. Silva MVDA, Faroni LRDA, de Alencar ER, de Sousa AH, Cecon PR, Nogueira JVF, Mason Filho V (2022) Ozone injection at low pressure: decomposition kinetics, control of Sitophilus zeamais, and popcorn kernel quality. Ozone-Sci Eng 44(1):66–78. https://doi.org/10.1080/01919512.2021.1937043

    Article  CAS  Google Scholar 

  20. Parish ME, Beuchat LR, Suslow TV, Harris LJ, Garrett EH, Farber JN, Busta FF (2003) Methods to reduce/eliminate pathogens from fresh and fresh-cut produce. Compr Rev Food Sci Food Saf 2:161–173

    Article  Google Scholar 

  21. King BS, Page EH, Mueller CA, Dollberg DD, Gomez KE, Warren AM (2006) Eye and respiratory symptoms in poultry processing workers exposed to chlorine by-products. Am J Ind Med 49(2):119–126. https://doi.org/10.1002/ajim.20259

    Article  CAS  PubMed  Google Scholar 

  22. Cardador MJ, Gallego M (2018) Determination of several common disinfection by-products in frozen foods. Food Addit Contam A 35(1):56–65. https://doi.org/10.1080/19440049.2017.1382731

    Article  CAS  Google Scholar 

  23. Pandiselvam R, Subhashini S, BanuuPriya EP, Kothakota A, Ramesh SV, Shahir S (2019) Ozone based food preservation: a promising green technology for enhanced food safety. Ozone: Sci Eng 41(1):17–34. https://doi.org/10.1080/01919512.2021.1904204

    Article  CAS  Google Scholar 

  24. Pandiselvam R, Thirupathi V (2015) Reaction kinetics of ozone gas in green gram (Vigna radiate). Ozone-Sci Eng 37(4):309–315. https://doi.org/10.1080/01919512.2014.984158

    Article  CAS  Google Scholar 

  25. Pandiselvam R, Sunoj S, Manikantan MR, Kothakota A, Hebbar KB (2017) Application and kinetics of ozone in food preservation. Ozone-Sci Eng 39(2):115–126. https://doi.org/10.1080/01919512.2016.1268947

    Article  CAS  Google Scholar 

  26. Korany AM, Hua Z, Green T, Hanrahan I, El-Shinawy SH, El-Kholy A, Hassan G, Zhu MJ (2018) Efficacy of ozonated water, chlorine, chlorine dioxide, quaternary ammonium compounds and peroxyacetic acid against Listeria monocytogenes biofilm on polystyrene surfaces. Front Microbiol 9:2296. https://doi.org/10.3389/fmicb.2018.02296

    Article  PubMed  PubMed Central  Google Scholar 

  27. Harada AMM, Nascimento MS (2021) Effect of dry sanitizing methods on Bacillus cereus biofilm. Braz J Microbiol 52(2):919–926. https://doi.org/10.1007/2Fs42770-021-00451-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Cárdenas FC, Andres S, Giannuzzi L, Zaritzky N (2011) Antimicrobial action and effects on beef quality attributes of a gaseous ozone treatment at refrigeration temperatures. Food Cont 22(8):1442–1447. https://doi.org/10.1016/j.foodcont.2011.03.006

    Article  CAS  Google Scholar 

  29. 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(7):1484. https://doi.org/10.3390/foods10071484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Kanaan MH (2018) Antibacterial effect of ozonated water against methicillin-resistant Staphylococcus aureus contaminating chicken meat in Wasit Province Iraq. Vet World 11(10):1445. https://doi.org/10.14202/vetworld.2018.1445-1453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Torlak E, Sert D, Ulca P (2013) Efficacy of gaseous ozone against Salmonella and microbial population on dried oregano. Int J Food Microbiol 165(3):276–280. https://doi.org/10.1016/j.ijfoodmicro.2013.05.030

    Article  CAS  PubMed  Google Scholar 

  32. Rezende AJ, de Alencar ER, Ferreira MDA, Ferreira WFDS (2021) Control of Listeria monocytogenes in refrigerated ozonated water. Ozone-Sci Eng 44(3):281–290. https://doi.org/10.1080/01919512.2021.1912586

    Article  CAS  Google Scholar 

  33. Rodrigues RS, Machado SG, de Carvalho AF, Nero LA (2021) Pseudomonas sp. as the causative agent of anomalous blue discoloration in Brazilian fresh soft cheese (Minas Frescal). Int Dairy J 117:105020. https://doi.org/10.1016/j.idairyj.2021.105020

    Article  CAS  Google Scholar 

  34. Chierici M, Picozzi C, La Spina MG, Orsi C, Vigentini I, Zambrini V, Foschino R (2016) Strain diversity of Pseudomonas fluorescens group with potential blue pigment phenotype isolated from dairy products. J Food Prot 79(8):1430–1435. https://doi.org/10.4315/0362-028X.JFP-15-589

    Article  CAS  PubMed  Google Scholar 

  35. Swanson KMJ, Petran RL, Hanlin JH (2015) Culture methods for enumeration of microorganisms Compendium of methods for the microbiological examination of foods. Am Pub Health Assoc 4:53–62. https://doi.org/10.2105/MBEF.0222

    Article  Google Scholar 

  36. Kang C, Xiang Q, Zhao D, Wang W, Niu L, Bai Y (2019) Inactivation of Pseudomonas deceptionensis CM2 on chicken breasts using plasma-activated water. J Food Sci Tech 56:4938–4945. https://doi.org/10.1007/s13197-019-03964-7

    Article  CAS  Google Scholar 

  37. Machado SG, da Silva FL, Bazzolli DM, Heyndrickx M, Costa PMDA, Vanetti MCD (2015) Pseudomonas spp. and Serratia liquefaciens as predominant spoilers in cold raw milk. J Food Sci 80(8):1842–1849. https://doi.org/10.1111/1750-3841.12957

    Article  CAS  Google Scholar 

  38. Asawanonda P, Taylor CR (1999) Wood’s light in dermatology. Int J Dermatol 38(11):801–807. https://doi.org/10.1046/j.1365-4362.1999.00794.x

    Article  CAS  PubMed  Google Scholar 

  39. Francis FJ (1975) The original of tan-1a/b. J Food Sci 40:412

    Article  Google Scholar 

  40. Little A (1975) A research note on a tangent. J Food Sci 40(2):410

    Article  Google Scholar 

  41. McLellan MR, Lind LR, Kime RW (1995) Hue angle determinations and statistical analysis for muiltquadrant hinter, L, a, b data. J Food Qual 18(3):235–240. https://doi.org/10.1111/j.1745-4557.1995.tb00377.x

    Article  Google Scholar 

  42. Gardoni D, Vailati A, Canziani R (2012) Decay of ozone in water: a review. Ozone: Sci Eng 34(4):233–242. https://doi.org/10.1080/01919512.2012.686354

    Article  CAS  Google Scholar 

  43. Christensen PA, Yonar T, Zakaria K (2013) The electrochemical generation of ozone: a review. Ozone: Sci Eng 35(3):149–167. https://doi.org/10.1080/01919512.2013.761564

    Article  CAS  Google Scholar 

  44. Galdeano MC, Wilhelm AE, Goulart IB, Tonon RV, Freitas-Silva O, Germani R, Chávez DWH (2018) Effect of water temperature and pH on the concentration and time of ozone saturation. Braz J Food Technol 21:e2017156. https://doi.org/10.1590/1981-6723.15617

    Article  CAS  Google Scholar 

  45. Shao L, Dong Y, Chen X, Xu X, Wang H (2020) Modeling the elimination of mature biofilms formed by Staphylococcus aureus and Salmonella spp Using combined ultrasound and disinfectants. Ult Sonoch 69:105269. https://doi.org/10.1016/j.ultsonch.2020.105269

    Article  CAS  Google Scholar 

  46. 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(1):162. https://doi.org/10.3390/microorganisms10010162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Khadre MA, Yousef AE, Kim JG (2001) Microbiological aspects of ozone applications in food: a review. J Food Sci 66(9):1242–1252. https://doi.org/10.1111/j.1365-2621.2001.tb15196.x

    Article  CAS  Google Scholar 

  48. Souza SMO, de Alencar ER, Ribeiro JL, de Aguiar Ferreira M (2019) Inactivation of Escherichia coli O157:H7 by ozone in different substrates. Braz J Microbiol 50(1):247–253. https://doi.org/10.1007/s42770-018-0025-2

    Article  CAS  Google Scholar 

  49. Meyer JM (2000) Pyoverdines: pigments, siderophores and potential taxonomic markers of fluorescent Pseudomonas species. Arch Microbiol 174(3):135–142. https://doi.org/10.1007/s002030000188

    Article  CAS  PubMed  Google Scholar 

  50. Castell‐Perez, ME, Moreira, RG (2004) Decontamination systems. Preharvest and postharvest food safety: contemporary issues and future directions, 337–348. https://doi.org/10.1002/9780470752579.ch25

  51. Cullen PJ, Tiwari BK, O’Donnell CP, Muthukumarappan K (2009) Modelling approaches to ozone processing of liquid foods. Trends in Food Sci Technol 20(3–4):125–136. https://doi.org/10.1016/j.tifs.2009.01.049

    Article  CAS  Google Scholar 

  52. Lee SK, Chon JW, Yun YK, Lee JC, Jo C, Song KY, Kim DH, Bae D, Kim H, Moon JS, Seo KH (2022) Properties of broiler breast meat with pale color and a new approach for evaluating meat freshness in poultry processing plants. Poult Sci 101(3):101627. https://doi.org/10.1016/j.psj.2021.101627

    Article  CAS  PubMed  Google Scholar 

  53. AMSA. American Meat Science Association (2012) AMSA meat color measurement guidelines. AMSA, Champaign. https://meatscience.org/docs/default-source/publications-resources/hottopics/2012_12_meat_clr_guide.pdf

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Funding

The authors acknowledge the support from the National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq, Grant Number: 405894/2021–0 and 406719/2023-3), the Research Support Foundation of the State of Minas Gerais (Fundação de Amparo à Pesquisa do Estado de Minas Gerais, FAPEMIG, Grant Number: APQ-00088–21 and APQ-01701–22), the Coordination for the Improvement of Higher Education Personnel (Coordenação de Aperfeiçoamento de Pessoal de Nível de Superior, CAPES), Funding Code 001, FARA, and Tertiary Education Trust Fund (TetFund).

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EAO, ERA, LRDF, and SGM conceived and designed the experiment. EAO, ERA, SGM, LRDF, MVAS, AF, and NASC performed the experiments and analyzed the data. EAO, ERA, LRDF, and SGM wrote the manuscript. EAO, ERA, LRDF, and SGM revised the manuscript. ERA, LRDF, and SGM provided the funding for the study.

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Correspondence to Ernandes Rodrigues de Alencar.

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Okolo, E.A., de Alencar, E.R., Machado, S.G. et al. Ozonation for Pseudomonas paracarnis control: biofilm removal and preservation of chicken meat during refrigerated storage. Braz J Microbiol 54, 3051–3060 (2023). https://doi.org/10.1007/s42770-023-01157-1

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