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Determination of Ozone Gas Effectiveness as Antifungal Agent

Year 2021, Issue: 26, 40 - 48, 29.08.2021

Beyza Arda Elif Onbaşı Ayşe Öztürk Aycan Cinar

Abstract

Abstract


Objective: Molds and yeasts which are predominant microorganisms in the air of food facility, contaminate foods through airborne and cause microbial spoilage. In addition to their adverse effects on food quality, molds produce mycotoxins which have toxic effects on humans and animals. Nowadays, ozone (O3) applications appear as a green technology used mold prevention and detoxification method in food industry. In this study, the antifungal activity of O3 gas was determined in a controlled air environment.

Material and methods: 0,5 McFarland yeast (Candida parapsilosis, Schizosaccharomyces pombe, Saccharomyces cerevisiae) and mold spore (Aspergillus flavus, Aspergillus parasiticus, Penicillium digitatum, Penicillium expansum, Penicillium roqueforti) suspensions were sprayed into 250 L airtight test cabin and exposed to ozone gas (10.000 mg/hour) for 3, 5, 10 min. Antifungal activity was determined by comparing the number of microorganisms by active- passive sampling before and after ozone application.

Results and conclusion: 100% antifungal effect was detected in all tested microorganisms with 3 minutes of ozone application.

Keywords

Ozone Air Yeast Mold Antifungal Activity Food Spoilage

References

  • Adebo, O.A., Molelekoa, T., Makhuvele, R., Adebiyi, J.A., Oyedeji, A.B., Gbashi, S. and Njobeh, P.B. (2021). A review on novel non‐thermal food processing techniques for mycotoxin reduction. International Journal of Food Science & Technology, 56(1) :13-27.
  • Alshannaq, A. and Yu, J.H. (2017). Occurrence, toxicity, and analysis of major mycotoxins in food. International Journal of Environmental Research and Public Health, 14(6) :632.
  • Alwi, N.A., and Ali, A. (2014). Reduction of Escherichia coli O157, Listeria monocytogenes and Salmonella enterica sv. Typhimurium populations on fresh-cut bell pepper using gaseous ozone. Food Control, 46: 304-311.
  • Ames, Z.R., Feliziani, E., and Smilanick, J.L. (2013). Germination of fungal conidia after exposure to low concentration ozone atmospheres. Postharvest Biology and Technology, 83:22–26.
  • Arendrup, M.C., Howard, S., Lass-Florl, C., Mouton, J.W., Meletiadis, J. and CuencaEstrella, M. (2014). EUCAST testing of isavuconazole susceptibility in Aspergillus: Comparison of results for inoculum standardization using conidium counting versus optical density. Antimicrobial Agents and Chemotherapy, 58: 6432-6436.
  • Asokapandian, S., Periasamy, S., and Swamy, G.J. (2018). Ozone for fruit juice preservation. In Fruit juices. Academic Press, s. 511-527.
  • Chukwudi, U.P., Kutu, F.R., and Mavengahama, S. (2021). Mycotoxins in Maize and Implications on Food Security: A Review. Agricultural Reviews, 42(1).
  • Cinar, A., and Onbaşı, E. (2020). Mycotoxins: The hidden danger in foods. In Mycotoxins and food safety. IntechOpen, s. 43-65, Londan, UK.
  • Çatal, H. ve İbanoğlu, Ş. (2010). Gıdaların Ozonlanması. Gıda Teknolojileri Elektronik Dergisi, 5: 47-55.
  • Çınar, S., Yılmaz, S.N., Aydın, E. ve Yorulmaz, A. (2017). Gıda ve Yem İçin Hızlı Alarm Sistemi (RASFF) 2009-2016 Türkiye Raporu. Türk Tarım – Gıda Bilim ve Teknoloji Dergisi, 5(8) : 873-882.
  • Da Rocha, M.E.B., Freire, F.D.C.O., Maia, F.E.F., Guedes, M.I.F. and Rondina, D. (2014). Mycotoxins and their effects on human and animal health. Food Control, 36(1): 159-165.
  • De Oliveira, J.M., de Alencar, E.R., Blum, L.E.B., de Souza Ferreira, W.F., Botelho, S.D.C.C., Racanicci, A.M.C. and da Silva, C.R. (2020). Ozonation of Brazil nuts: Decomposition kinetics, control of Aspergillus flavus and the effect on color and on raw oil quality. LWT, 123 :109106.
  • Eryılmaz, D. (2015). Mikrobiyal Hava Toplayıcı ve Okuyucu Sistemi Tasarımı ve Prototip Üretimi. Biyomühendislik Bölümü, Ankara. https://tez.yok.gov.tr/UlusalTezMerkezi/tezSorguSonucYeni.jsp, (Accessed: 06.05.2021)
  • Escrivá, L., Oueslati, S., Font, G. and Manyes, L. (2017). Alternaria mycotoxins in food and feed: An overview. Journal of Food Quality, 1–20.
  • EUCAST, (2015). Method for susceptibility testing of moulds; For the determination of broth dilution minimum inhibitory concentrations of antifungal agents for conidia forming moulds. Copenhagen, Denmark.
  • FAO, (2017). Food and Agriculture Organization of the United Nations. Save Food: Global Initiative on Food Loss and Waste Reduction—Key Findings. http://www.fao.org/save-food/resources/keyfindings/en/ (Accessed 20.04.2021).
  • FDA, (2021). Recalls, Market Withdrawals, & Safety Alerts. https://www.fda.gov/safety/recalls-market-withdrawals-safety-alerts (Accessed 01.05.2021).
  • Fernandes, T.H. (2017). Mycotoxins, food and health mycotoxins, food and health. Journal of Nutritional Health & Food Science, 5(7) :1-10.
  • Ferrão, J., Bell, V., Chabite, I.T. and Fernandes, T.H. (2017). Mycotoxins, food and health mycotoxins, food and health. Journal of Nutritional Health & Food Science, 5(7) :1-10.
  • Günaydın, Ş. ve Karaca, H. (2015). Küf gelişimi ve mikotoksin oluşumunun kontrolünde doğal bitki ekstraktlarının kullanımı. Akademik Gıda, 13(2) :173-182.
  • Kitinoja, L., Saran, S., Roy, S.K. and Kader, A.A. (2011). Postharvest technology for developing countries: Challenges and opportunities in research, outreach and advocacy. Journal of the Science of Food and Agriculture, 91: 597–603.
  • Leyva Salas, M., Mounier, J., Valence, F., Coton, M., Thierry, A. and Coton, E. (2017). Antifungal microbial agents for food biopreservation—a review. Microorganisms, 5(3) :37.
  • Loncar, J., Bellich, B., Parroni, A., Reverberi, M., Rizzo, R., Zjalić, S. and Cescutti, P. (2021). Oligosaccharides Derived from Tramesan: Their Structure and Activity on Mycotoxin Inhibition in Aspergillus flavus and Aspergillus carbonarius. Biomolecules, 11(2) :243.
  • Luo, Y., Liu, X. and Li, J. (2018). Updating Techniques on Controlling mycotoxins-A Review. Food Control, 89 :123–132.
  • Masotti, F., Vallone, L., Ranzini, S., Silvetti, T., Morandi, S. and Brasca, M. (2019). Effectiveness of air disinfection by ozonation or hydrogen peroxide aerosolization in dairy environments. Food Control, 97 :32-38.
  • NCCLS, (2002).National Committee for Clinical and Laboratory Standards. M27-A2 Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts. 22: 15.
  • Oğuz, H. (2017). Mikotoksinler ve Önemi. Turkiye Klinikleri Veterinary Sciences Pharmacology and Toxicology, 3(2) :113-119.
  • Pandiselvam, R., Subhashini, S., Banuu Priya, E., Kothakota, A., Ramesh, S. and Shahir, S. (2019). Ozone Based Food Preservation: A Promising Green Technology for Enhanced Food Safety. Ozone: Science and Engineering, 41(1) :17–34.
  • Rodriguez-Tudela, J.L., Chryssanthou, E., Petrikkou, E., Mosquera, J., Denning, D.W. and Cuenca-Estrella, M. (2003). Interlaboratory evaluation of hematocytometer method of inoculum preparation for testing antifungal susceptibilities of filamentous fungi. Journal Clinic Microbiology, 41 :5236-5237.
  • Savi, G.D. and Scussel, V.M. (2014). Effects of Ozone Gas Exposure on Toxigenic Fungi Species from Fusarium, Aspergillus, and Penicillium Genera. Ozone: Science & Engineering, 36(2) :144–152.
  • Serra, R., Abrunhosa, L., Kozakiewicz, Z., Venâncio, A. and Lima, N. (2003). Use of ozone to reduce molds in a cheese ripening room. Journal of Food Protection, 66(12) :2355-2358.
  • Silva, J.V.B.D., Oliveira, C.A.F.D. and Ramalho, L.N.Z. (2021). An overview of mycotoxins, their pathogenic effects, foods where they are found and their diagnostic biomarkers. Food Science and Technology, (AHEAD).
  • Snyder, A.B. and Worobo, R.W. (2018a). The incidence and impact of microbial spoilage as reported by juice manufacturers. Food Control, 85 :144–150.
  • Snyder, A.B. and Worobo, R.W. (2018b). Fungal spoilage in food processing. Journal of food protection, 81(6) :1035-1040.
  • Vallone, L. and Stella, S. (2014). Evaluation of antifungal effect of gaseous ozone in a meat processing plant. Italian Journal of Food Safety, 3(2).
  • World Health Organization (WHO), (2018). Mycotoxins. https://www.who.int/news-room/ fact-sheets/detail/mycotoxins, (Accessed 20.04.2021).
  • Yalçın, S. ve Alçay, A. Ü. (2015). İç Ortam Havası Biyoaerosolleri ve mikrobiyal hava kalitesi ölçüm metodları. Anadolu Bil Meslek Yüksekokulu Dergisi, (37) :17-30.
  • Zorlugenç, B., Zorlugenç, F.K., Öztekin, S. and Evliya, I.B. (2008). The influence of gaseous ozone and ozonated water on microbial flora and degradation of Aflatoxin B1 in dried figs. Food and Chemical Toxicology 46(12) :3593-3597.

Ozon Gazının Antifungal Ajan Olarak Etkinliğinin Belirlenmesi

Year 2021, Issue: 26, 40 - 48, 29.08.2021

Beyza Arda Elif Onbaşı Ayşe Öztürk Aycan Cinar

Abstract

Özet

Amaç: Gıda işletmelerinde ortam havasında baskın olarak bulunan küf ve mayalar, hava kaynaklı kontaminasyon yoluyla gıdalara bulaşmakta ve mikrobiyal bozulmalara neden olmaktadır. Küfler gıda kalitesi üzerindeki olumsuz etkilerinin ötesinde, insanlar ve hayvanlar üzerinde toksik etkiye sahip mikotoksin adı verilen ikincil metabolitler üretmektedir. Günümüzde ozon (O3) uygulamaları gıda sanayinde küf önleyici ve detoksifikasyon yöntemi olarak kullanılan yeşil teknoloji olarak karşımıza çıkmaktadır. Bu çalışmada kontrollü hava ortamında O3 gazının antifungal etkinliği belirlenmiştir.

Materyal ve yöntem: 0,5 McFarland’a ayarlanmış maya (Candida parapsilosis, Schizosaccharomyces pombe, Saccharomyces cerevisiae) ve küf sporu (Aspergillus flavus, Aspergillus parasiticus, Penicillium digitatum, Penicillium expansum, Penicillium roqueforti) süspansiyonu 250 L hava sızdırmaz özellikteki test kabini içine püskürtülerek; 3, 5 ile 10 dk ozon gazına (10.000 mg/saat) maruz bırakılmıştır. Ozon uygulama öncesi ve sonrası aktif ve pasif örnekleme yapılarak mikroorganizma sayıları kıyaslanarak antifungal etkinlik belirlenmiştir.

Bulgular ve sonuç: 3 dk ozon uygulaması ile test edilen tüm mikroorganizmalarda gelişmenin %100 engellendiği tespit edilmiştir.

Keywords

Ozone Air Yeast Mold Antifungal Activity Food Spoilage Ozone, Air, Yeast, Mold, Antifungal Activity, Food Spoilage

References

  • Adebo, O.A., Molelekoa, T., Makhuvele, R., Adebiyi, J.A., Oyedeji, A.B., Gbashi, S. and Njobeh, P.B. (2021). A review on novel non‐thermal food processing techniques for mycotoxin reduction. International Journal of Food Science & Technology, 56(1) :13-27.
  • Alshannaq, A. and Yu, J.H. (2017). Occurrence, toxicity, and analysis of major mycotoxins in food. International Journal of Environmental Research and Public Health, 14(6) :632.
  • Alwi, N.A., and Ali, A. (2014). Reduction of Escherichia coli O157, Listeria monocytogenes and Salmonella enterica sv. Typhimurium populations on fresh-cut bell pepper using gaseous ozone. Food Control, 46: 304-311.
  • Ames, Z.R., Feliziani, E., and Smilanick, J.L. (2013). Germination of fungal conidia after exposure to low concentration ozone atmospheres. Postharvest Biology and Technology, 83:22–26.
  • Arendrup, M.C., Howard, S., Lass-Florl, C., Mouton, J.W., Meletiadis, J. and CuencaEstrella, M. (2014). EUCAST testing of isavuconazole susceptibility in Aspergillus: Comparison of results for inoculum standardization using conidium counting versus optical density. Antimicrobial Agents and Chemotherapy, 58: 6432-6436.
  • Asokapandian, S., Periasamy, S., and Swamy, G.J. (2018). Ozone for fruit juice preservation. In Fruit juices. Academic Press, s. 511-527.
  • Chukwudi, U.P., Kutu, F.R., and Mavengahama, S. (2021). Mycotoxins in Maize and Implications on Food Security: A Review. Agricultural Reviews, 42(1).
  • Cinar, A., and Onbaşı, E. (2020). Mycotoxins: The hidden danger in foods. In Mycotoxins and food safety. IntechOpen, s. 43-65, Londan, UK.
  • Çatal, H. ve İbanoğlu, Ş. (2010). Gıdaların Ozonlanması. Gıda Teknolojileri Elektronik Dergisi, 5: 47-55.
  • Çınar, S., Yılmaz, S.N., Aydın, E. ve Yorulmaz, A. (2017). Gıda ve Yem İçin Hızlı Alarm Sistemi (RASFF) 2009-2016 Türkiye Raporu. Türk Tarım – Gıda Bilim ve Teknoloji Dergisi, 5(8) : 873-882.
  • Da Rocha, M.E.B., Freire, F.D.C.O., Maia, F.E.F., Guedes, M.I.F. and Rondina, D. (2014). Mycotoxins and their effects on human and animal health. Food Control, 36(1): 159-165.
  • De Oliveira, J.M., de Alencar, E.R., Blum, L.E.B., de Souza Ferreira, W.F., Botelho, S.D.C.C., Racanicci, A.M.C. and da Silva, C.R. (2020). Ozonation of Brazil nuts: Decomposition kinetics, control of Aspergillus flavus and the effect on color and on raw oil quality. LWT, 123 :109106.
  • Eryılmaz, D. (2015). Mikrobiyal Hava Toplayıcı ve Okuyucu Sistemi Tasarımı ve Prototip Üretimi. Biyomühendislik Bölümü, Ankara. https://tez.yok.gov.tr/UlusalTezMerkezi/tezSorguSonucYeni.jsp, (Accessed: 06.05.2021)
  • Escrivá, L., Oueslati, S., Font, G. and Manyes, L. (2017). Alternaria mycotoxins in food and feed: An overview. Journal of Food Quality, 1–20.
  • EUCAST, (2015). Method for susceptibility testing of moulds; For the determination of broth dilution minimum inhibitory concentrations of antifungal agents for conidia forming moulds. Copenhagen, Denmark.
  • FAO, (2017). Food and Agriculture Organization of the United Nations. Save Food: Global Initiative on Food Loss and Waste Reduction—Key Findings. http://www.fao.org/save-food/resources/keyfindings/en/ (Accessed 20.04.2021).
  • FDA, (2021). Recalls, Market Withdrawals, & Safety Alerts. https://www.fda.gov/safety/recalls-market-withdrawals-safety-alerts (Accessed 01.05.2021).
  • Fernandes, T.H. (2017). Mycotoxins, food and health mycotoxins, food and health. Journal of Nutritional Health & Food Science, 5(7) :1-10.
  • Ferrão, J., Bell, V., Chabite, I.T. and Fernandes, T.H. (2017). Mycotoxins, food and health mycotoxins, food and health. Journal of Nutritional Health & Food Science, 5(7) :1-10.
  • Günaydın, Ş. ve Karaca, H. (2015). Küf gelişimi ve mikotoksin oluşumunun kontrolünde doğal bitki ekstraktlarının kullanımı. Akademik Gıda, 13(2) :173-182.
  • Kitinoja, L., Saran, S., Roy, S.K. and Kader, A.A. (2011). Postharvest technology for developing countries: Challenges and opportunities in research, outreach and advocacy. Journal of the Science of Food and Agriculture, 91: 597–603.
  • Leyva Salas, M., Mounier, J., Valence, F., Coton, M., Thierry, A. and Coton, E. (2017). Antifungal microbial agents for food biopreservation—a review. Microorganisms, 5(3) :37.
  • Loncar, J., Bellich, B., Parroni, A., Reverberi, M., Rizzo, R., Zjalić, S. and Cescutti, P. (2021). Oligosaccharides Derived from Tramesan: Their Structure and Activity on Mycotoxin Inhibition in Aspergillus flavus and Aspergillus carbonarius. Biomolecules, 11(2) :243.
  • Luo, Y., Liu, X. and Li, J. (2018). Updating Techniques on Controlling mycotoxins-A Review. Food Control, 89 :123–132.
  • Masotti, F., Vallone, L., Ranzini, S., Silvetti, T., Morandi, S. and Brasca, M. (2019). Effectiveness of air disinfection by ozonation or hydrogen peroxide aerosolization in dairy environments. Food Control, 97 :32-38.
  • NCCLS, (2002).National Committee for Clinical and Laboratory Standards. M27-A2 Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts. 22: 15.
  • Oğuz, H. (2017). Mikotoksinler ve Önemi. Turkiye Klinikleri Veterinary Sciences Pharmacology and Toxicology, 3(2) :113-119.
  • Pandiselvam, R., Subhashini, S., Banuu Priya, E., Kothakota, A., Ramesh, S. and Shahir, S. (2019). Ozone Based Food Preservation: A Promising Green Technology for Enhanced Food Safety. Ozone: Science and Engineering, 41(1) :17–34.
  • Rodriguez-Tudela, J.L., Chryssanthou, E., Petrikkou, E., Mosquera, J., Denning, D.W. and Cuenca-Estrella, M. (2003). Interlaboratory evaluation of hematocytometer method of inoculum preparation for testing antifungal susceptibilities of filamentous fungi. Journal Clinic Microbiology, 41 :5236-5237.
  • Savi, G.D. and Scussel, V.M. (2014). Effects of Ozone Gas Exposure on Toxigenic Fungi Species from Fusarium, Aspergillus, and Penicillium Genera. Ozone: Science & Engineering, 36(2) :144–152.
  • Serra, R., Abrunhosa, L., Kozakiewicz, Z., Venâncio, A. and Lima, N. (2003). Use of ozone to reduce molds in a cheese ripening room. Journal of Food Protection, 66(12) :2355-2358.
  • Silva, J.V.B.D., Oliveira, C.A.F.D. and Ramalho, L.N.Z. (2021). An overview of mycotoxins, their pathogenic effects, foods where they are found and their diagnostic biomarkers. Food Science and Technology, (AHEAD).
  • Snyder, A.B. and Worobo, R.W. (2018a). The incidence and impact of microbial spoilage as reported by juice manufacturers. Food Control, 85 :144–150.
  • Snyder, A.B. and Worobo, R.W. (2018b). Fungal spoilage in food processing. Journal of food protection, 81(6) :1035-1040.
  • Vallone, L. and Stella, S. (2014). Evaluation of antifungal effect of gaseous ozone in a meat processing plant. Italian Journal of Food Safety, 3(2).
  • World Health Organization (WHO), (2018). Mycotoxins. https://www.who.int/news-room/ fact-sheets/detail/mycotoxins, (Accessed 20.04.2021).
  • Yalçın, S. ve Alçay, A. Ü. (2015). İç Ortam Havası Biyoaerosolleri ve mikrobiyal hava kalitesi ölçüm metodları. Anadolu Bil Meslek Yüksekokulu Dergisi, (37) :17-30.
  • Zorlugenç, B., Zorlugenç, F.K., Öztekin, S. and Evliya, I.B. (2008). The influence of gaseous ozone and ozonated water on microbial flora and degradation of Aflatoxin B1 in dried figs. Food and Chemical Toxicology 46(12) :3593-3597.
There are 38 citations in total.

Details

Primary Language Turkish
Journal Section Journal of Food and Feed Science-Technology
Authors

Beyza Arda This is me 0000-0003-3193-0270

Elif Onbaşı 0000-0002-5169-7392

Ayşe Öztürk This is me 0000-0001-8286-706X

Aycan Cinar This is me 0000-0003-2038-725X

Publication Date August 29, 2021
Published in Issue Year 2021 Issue: 26

Cite

APA Arda, B., Onbaşı, E., Öztürk, A., Cinar, A. (2021). Ozon Gazının Antifungal Ajan Olarak Etkinliğinin Belirlenmesi. Gıda Ve Yem Bilimi Teknolojisi Dergisi(26), 40-48.
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