Cold plasma: exploring a new option for management of postharvest fungal pathogens, mycotoxins and insect pests in Australian stored cereal grain
M. Kaur A , D. Hüberli B and K. L. Bayliss A CA College of Science, Health, Engineering and Education, Murdoch University, 90 South Street, Murdoch, WA 6150, Australia.
B Department of Primary Industries and Regional Development, 3 Baron-Hay Court, South Perth, WA 6151, Australia.
C Corresponding author. Email: K.Bayliss@murdoch.edu.au
Crop and Pasture Science 71(8) 715-724 https://doi.org/10.1071/CP20078
Submitted: 19 March 2020 Accepted: 16 July 2020 Published: 13 August 2020
Abstract
Various strategies are used to reduce postharvest cereal grain contaminants such as insect pests and fungal pathogens. Chemical and physical treatments are common management practices but may leave harmful chemical residues on grains or alter their nutrient content (particularly temperature treatments) and have other limitations. This review explores the recent literature regarding cold plasma, with emphasis on its efficacy for decontamination of postharvest cereal grain from biological contaminants. Cold plasma is an ionised gas containing reactive oxygen and nitrogen species, electrons and free radicals that are lethal to microorganisms and has the potential to decontaminate food surfaces and to increase shelf life. Studies conducted on rice, wheat, corn, barley and oats have demonstrated that cold plasma significantly reduced the amount of fungi, bacteria and their spores on grain surfaces. Cold plasma may also detoxify mycotoxins, and control insect pests. Evidence from various global studies demonstrates the potential use of cold plasma to manage postharvest fungi, mycotoxins and insect pests in Australian stored cereal grain.
Additional keywords: detoxification, grain quality, inactivation, mould.
References
Abd El-Aziz MF, Mahmoud EA, Elaragi GM (2014) Non thermal plasma for control of the Indian meal moth, Plodia interpunctella (Lepidoptera: Pyralidae). Journal of Stored Products Research 59, 215–221.| Non thermal plasma for control of the Indian meal moth, Plodia interpunctella (Lepidoptera: Pyralidae).Crossref | GoogleScholarGoogle Scholar |
Anonymous (2019) Grain storage: maintaining grain quality. Available at https://www.agric.wa.gov.au/barley/grain-storage-maintaining-grain-quality (accessed 30 July 2020).
Bahrami N, Bayliss D, Chope G, Penson S, Perehinec T, Fisk ID (2016) Cold plasma: a new technology to modify wheat flour functionality. Food Chemistry 202, 247–253.
| Cold plasma: a new technology to modify wheat flour functionality.Crossref | GoogleScholarGoogle Scholar | 26920291PubMed |
Basaran P, Basaran-Akgul N, Oksuz L (2008) Elimination of Aspergillus parasiticus from nut surface with low pressure cold plasma (LPCP) treatment. Food Microbiology 25, 626–632.
| Elimination of Aspergillus parasiticus from nut surface with low pressure cold plasma (LPCP) treatment.Crossref | GoogleScholarGoogle Scholar | 18456118PubMed |
Bourke P, Ziuzina D, Han L, Cullen PJ, Gilmore BF (2017) Microbiological interactions with cold plasma. Journal of Applied Microbiology 123, 308–324.
| Microbiological interactions with cold plasma.Crossref | GoogleScholarGoogle Scholar | 28245092PubMed |
Bourke P, Ziuzina D, Boehm D, Cullen PJ, Keener K (2018) The potential of cold plasma for safe and sustainable food production. Trends in Biotechnology 36, 615–626.
| The potential of cold plasma for safe and sustainable food production.Crossref | GoogleScholarGoogle Scholar | 29329724PubMed |
Braşoveanu M, Nemţanu M, Surdu-Bob C, Karaca G, Erper I (2015) Effect of glow discharge plasma on germination and fungal load of some cereal seeds. Romanian Reports in Physics 67, 617–624.
Brick NMM, Lorini I, Scussel VM (2006) Fungus and mycotoxins in wheat grain at post harvest. In ‘9th International Working Conference on Stored Product Protection’. Sao Paulo, Brazil, 15–18 October. (Brazilian Post-Harvest Association (ABRAPOS): Passo Fundo, Brazil)
Bullerman LB, Bianchini A (2007) Stability of mycotoxins during food processing. International Journal of Food Microbiology 119, 140–146.
| Stability of mycotoxins during food processing.Crossref | GoogleScholarGoogle Scholar | 17804104PubMed |
Butscher D, Zimmermann D, Schuppler M, Rudolf von Rohr P (2016) Plasma inactivation of bacterial endospores on wheat grains and polymeric model substrates in a dielectric barrier discharge. Food Control 60, 636–645.
| Plasma inactivation of bacterial endospores on wheat grains and polymeric model substrates in a dielectric barrier discharge.Crossref | GoogleScholarGoogle Scholar |
Carpen L, Chireceanu C, Teodorescu M, Chiriloaie A, Teodoru A, Dinescu G (2019) The effect of argon/oxygen and argon/nitrogen atmospheric plasma jet on stored products pests. Romanian Journal of Physics 64, 503–516.
Chen HH, Chen YK, Chang HC (2012) Evaluation of physicochemical properties of plasma treated brown rice. Food Chemistry 135, 74–79.
| Evaluation of physicochemical properties of plasma treated brown rice.Crossref | GoogleScholarGoogle Scholar |
Chen HH, Chang HC, Chen YK, Hung CL, Lin SY, Chen YS (2016) An improved process for high nutrition of germinated brown rice production: low-pressure plasma. Food Chemistry 191, 120–127.
| An improved process for high nutrition of germinated brown rice production: low-pressure plasma.Crossref | GoogleScholarGoogle Scholar | 26258710PubMed |
Chizoba Ekezie F-G, Sun D-W, Cheng J-H (2017) A review on recent advances in cold plasma technology for the food industry: current applications and future trends. Trends in Food Science & Technology 69, 46–58.
| A review on recent advances in cold plasma technology for the food industry: current applications and future trends.Crossref | GoogleScholarGoogle Scholar |
Collins P (2010) Research on stored product protection in Australia: a review of past, present and future directions. In ‘10th International Working Conference on Stored Product Protection’. (Julius-Kühn-Institut: Quedlinburg, Germany)
Cullen PJ, Lalor J, Scally L, Boehm D, Milosavljević V, Bourke P, Keener K (2018) Translation of plasma technology from the lab to the food industry. Plasma Processes and Polymers 15, 1700085–1700096.
| Translation of plasma technology from the lab to the food industry.Crossref | GoogleScholarGoogle Scholar |
Daglish GJ, Nayak MK (2018) Prevalence of resistance to deltamethrin in Rhyzopertha dominica (F.) in eastern Australia. Journal of Stored Products Research 78, 45–49.
| Prevalence of resistance to deltamethrin in Rhyzopertha dominica (F.) in eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Darby J, Caddick L (2007) Review of grain harvest bag technology under Australian conditions. CSIRO Entomology, Report No. 0643091130, Canberra, ACT, Australia.
Dasan BG, Boyaci IH, Mutlu M (2016) Inactivation of aflatoxigenic fungi (Aspergillus spp.) on granular food model, maize, in an atmospheric pressure fluidized bed plasma system. Food Control 70, 1–8.
| Inactivation of aflatoxigenic fungi (Aspergillus spp.) on granular food model, maize, in an atmospheric pressure fluidized bed plasma system.Crossref | GoogleScholarGoogle Scholar |
Devi Y, Thirumdas R, Sarangapani C, Deshmukh RR, Annapure US (2017) Influence of cold plasma on fungal growth and aflatoxins production on groundnuts. Food Control 77, 187–191.
| Influence of cold plasma on fungal growth and aflatoxins production on groundnuts.Crossref | GoogleScholarGoogle Scholar |
Drakulic J, Bruce T, Ray RV (2017) Direct and host‐mediated interactions between Fusarium pathogens and herbivorous arthropods in cereals. Plant Pathology 66, 3–13.
| Direct and host‐mediated interactions between Fusarium pathogens and herbivorous arthropods in cereals.Crossref | GoogleScholarGoogle Scholar |
Ehlbeck J, Schnabel U, Polak M, Winter J, Von Woedtke T, Brandenburg R, Von dem Hagen T, Weltmann K (2011) Low temperature atmospheric pressure plasma sources for microbial decontamination. Journal of Physics D, Applied Physics 44, 013002
| Low temperature atmospheric pressure plasma sources for microbial decontamination.Crossref | GoogleScholarGoogle Scholar |
Elmouttie D, Hamilton GS (2010) Review and gap analysis of stored grain sampling strategies. Cooperative Research Centre for National Plant Biosecurity, Australia. Available at: https://eprints.qut.edu.au/115088/1/crc30086_gap_analysis.pdf (accessed 30 July 2020).
Fields P, Allen S, Korunic Z, McLaughlin A, Stathers T (2003) Standardised testing for diatomaceous earth. In ‘Proceedings of the 8th International Conference on Stored-Product Protection’. York, UK, 22–26 July 2002. (CAB International: Wallingford, UK)
Gavahian M, Chu Y-H, Mousavi Khaneghah A, Barba FJ, Misra NN (2018) A critical analysis of the cold plasma induced lipid oxidation in foods. Trends in Food Science & Technology 77, 32–41.
| A critical analysis of the cold plasma induced lipid oxidation in foods.Crossref | GoogleScholarGoogle Scholar |
GRDC (2017) Grain storage. GrowNotes. Grains Research & Development Corporation, Canberra, ACT, Australia. Available at: https://grdc.com.au/resources-and-publications/grownotes/technical-manuals/grain-storage (accessed 30 July 2020).
GTA (2018) Australian Grain Industry – Code of Practice: Managing Severely Damaged Grain. Grain Trade Australia (GTA), Technical Guideline Document No. 12, Australia. Available at: http://www.graintrade.org.au/sites/default/files/file/Codes/Grain%20Industry%20Code%20of%20Practice/Technical%20Guidance%20Documents/TGD%20No_12%20Managing%20Severely%20Damaged%20Grain_May2018.pdf (accessed 30 July 2020).
Hagstrum DW, Phillips TW (2017) Evolution of stored-product entomology: protecting the world food supply. Annual Review of Entomology 62, 379–397.
| Evolution of stored-product entomology: protecting the world food supply.Crossref | GoogleScholarGoogle Scholar | 28141965PubMed |
Hayashi N, Yagyu Y, Yonesu A, Shiratani M (2014) Sterilization characteristics of the surfaces of agricultural products using active oxygen species generated by atmospheric plasma and UV light. Japanese Journal of Applied Physics 53, 05FR03
| Sterilization characteristics of the surfaces of agricultural products using active oxygen species generated by atmospheric plasma and UV light.Crossref | GoogleScholarGoogle Scholar |
Higgins J, McCue T (2010) ‘A strategic approach to storage. Ground Cover .Grain storage supplement.’ (Grains Research and Development Corporation: Canberra, ACT, Australia)
Hocking AD (2003) Microbiological facts and fictions in grain storage. In ‘Proceedings of the Australian Postharvest Technical Conference’. pp. 55–58. (CSIRO: Canberra, ACT, Australia)
Kim KH, Kabir E, Jahan SA (2017) Exposure to pesticides and the associated human health effects. Science of the Total Environment 575, 525–535.
| Exposure to pesticides and the associated human health effects.Crossref | GoogleScholarGoogle Scholar | 27614863PubMed |
Kogelschatz U (2004) Atmospheric-pressure plasma technology. Plasma Physics and Controlled Fusion 46, B63–B75.
| Atmospheric-pressure plasma technology.Crossref | GoogleScholarGoogle Scholar |
Kordas L, Pusz W, Czapka T, Kacprzyk R (2015) The effect of low-temperature plasma on fungus colonization of winter wheat grain and seed quality. Polish Journal of Environmental Studies 24, 433–438.
Laca A, Mousia Z, Díaz M, Webb C, Pandiella SS (2006) Distribution of microbial contamination within cereal grains. Journal of Food Engineering 72, 332–338.
| Distribution of microbial contamination within cereal grains.Crossref | GoogleScholarGoogle Scholar |
Laroussi M, Leipold F (2004) Evaluation of the roles of reactive species, heat, and UV radiation in the inactivation of bacterial cells by air plasmas at atmospheric pressure. International Journal of Mass Spectrometry 233, 81–86.
| Evaluation of the roles of reactive species, heat, and UV radiation in the inactivation of bacterial cells by air plasmas at atmospheric pressure.Crossref | GoogleScholarGoogle Scholar |
Los A, Ziuzina D, Akkermans S, Boehm D, Cullen PJ, Van Impe J, Bourke P (2018) Improving microbiological safety and quality characteristics of wheat and barley by high voltage atmospheric cold plasma closed processing. Food Research International 106, 509–521.
| Improving microbiological safety and quality characteristics of wheat and barley by high voltage atmospheric cold plasma closed processing.Crossref | GoogleScholarGoogle Scholar | 29579955PubMed |
Magan N, Hope R, Cairns V, Aldred D (2003) Post-harvest fungal ecology: impact of fungal growth and mycotoxin accumulation in stored grain. European Journal of Plant Pathology 109, 723–730.
| Post-harvest fungal ecology: impact of fungal growth and mycotoxin accumulation in stored grain.Crossref | GoogleScholarGoogle Scholar |
Magan N, Sanchis V, Aldred D (2004) Role of spoilage fungi in seed deterioration. In ‘Fungal biotechnology in agricultural, food and environmental applications’. (Ed. DK Arora) pp. 311–323. (Marcel Dekker: New York, USA)
Mannaa M, Kim KD (2017) Influence of temperature and water activity on deleterious fungi and mycotoxin production during grain storage. Mycobiology 45, 240–254.
| Influence of temperature and water activity on deleterious fungi and mycotoxin production during grain storage.Crossref | GoogleScholarGoogle Scholar | 29371792PubMed |
Mason LJ, McDonough M (2012) Biology, behavior, and ecology of stored grain and legume insects. In ‘Stored product protection’. (Eds DW Hagstrum, TW Phillips, G Cuperus) pp. 7–20. (Kansas State University: KS, USA)
Matthes R, Assadian O, Kramer A (2014) Repeated applications of cold atmospheric pressure plasma does not induce resistance in Staphylococcus aureus embedded in biofilms. GMS Hygiene and Infection Control 9, Doc17
Mesterházy Á, Oláh J, Popp J (2020) Losses in the grain supply chain: causes and solutions. Sustainability 12, 2342
| Losses in the grain supply chain: causes and solutions.Crossref | GoogleScholarGoogle Scholar |
Metz N (2009) The WA guide to high moisture harvest management, grain storage and handling. Cooperative Bulk Handling Group, Australia, pp. 1–68. Available at: http://www.giwa.org.au/_literature_133719/SEPWA_and_CBH_Group_-_the_WA_Guide_to_high_moisture_harvest_management_grain_storage_and_handling (accessed 30 July 2020).
Mir SA, Shah MA, Mir MM (2016) Understanding the role of plasma technology in food industry. Food and Bioprocess Technology 9, 734–750.
| Understanding the role of plasma technology in food industry.Crossref | GoogleScholarGoogle Scholar |
Mishenko AA, Malinin OA, Rashkovan VM, Basteev AV, Bazyma LA, Mazalov YP, Kutovoy VA (2000) Complex high-frequency technology for protection of grain against pests. Journal of Microwave Power and Electromagnetic Energy 35, 179–184.
| Complex high-frequency technology for protection of grain against pests.Crossref | GoogleScholarGoogle Scholar | 11098443PubMed |
Misra N, Tiwari B, Raghavarao K, Cullen P (2011) Nonthermal plasma inactivation of food-borne pathogens. Food Engineering Reviews 3, 159–170.
| Nonthermal plasma inactivation of food-borne pathogens.Crossref | GoogleScholarGoogle Scholar |
Misra NN, Kaur S, Tiwari BK, Kaur A, Singh N, Cullen PJ (2015) Atmospheric pressure cold plasma (ACP) treatment of wheat flour. Food Hydrocolloids 44, 115–121.
| Atmospheric pressure cold plasma (ACP) treatment of wheat flour.Crossref | GoogleScholarGoogle Scholar |
Morar R, Suarasan I, Budu S, Ghizdavu I, Porca M, Dascalescu L (1997) Corona discharge effects on some parasitical insects of cultured plants. Journal of Electrostatics 40–41, 669–673.
| Corona discharge effects on some parasitical insects of cultured plants.Crossref | GoogleScholarGoogle Scholar |
Mrema G, Gumbe L, Chepete H, Agullo J (2011) Grain crop drying, handling and storage. Rural Structures in the Tropics: Design and Development 3, 363–411.
Niemira BA (2012) Cold plasma decontamination of foods. Annual Review of Food Science and Technology 3, 125–142.
| Cold plasma decontamination of foods.Crossref | GoogleScholarGoogle Scholar | 22149075PubMed |
Ochi A, Konishi H, Ando S, Sato K, Yokoyama K, Tsushima S, Yoshida S, Morikawa T, Kaneko T, Takahashi H (2017) Management of bakanae and bacterial seedling blight diseases in nurseries by irradiating rice seeds with atmospheric plasma. Plant Pathology 66, 67–76.
| Management of bakanae and bacterial seedling blight diseases in nurseries by irradiating rice seeds with atmospheric plasma.Crossref | GoogleScholarGoogle Scholar |
Ouf SA, Basher AH, Mohamed AA (2015) Inhibitory effect of double atmospheric pressure argon cold plasma on spores and mycotoxin production of Aspergillus niger contaminating date palm fruits. Journal of the Science of Food and Agriculture 95, 3204–3210.
| Inhibitory effect of double atmospheric pressure argon cold plasma on spores and mycotoxin production of Aspergillus niger contaminating date palm fruits.Crossref | GoogleScholarGoogle Scholar | 25557283PubMed |
Park BJ, Takatori K, Sugita-Konishi Y, Kim I-H, Lee M-H, Han D-W, Chung K-H, Hyun SO, Park J-C (2007) Degradation of mycotoxins using microwave-induced argon plasma at atmospheric pressure. Surface and Coatings Technology 201, 5733–5737.
| Degradation of mycotoxins using microwave-induced argon plasma at atmospheric pressure.Crossref | GoogleScholarGoogle Scholar |
Pitt JI, Miller JD (2017) A concise history of mycotoxin research. Journal of Agricultural and Food Chemistry 65, 7021–7033.
| A concise history of mycotoxin research.Crossref | GoogleScholarGoogle Scholar | 27960261PubMed |
Ratish Ramanan K, Sarumathi R, Mahendran R (2018) Influence of cold plasma on mortality rate of different life stages of Tribolium castaneum on refined wheat flour. Journal of Stored Products Research 77, 126–134.
| Influence of cold plasma on mortality rate of different life stages of Tribolium castaneum on refined wheat flour.Crossref | GoogleScholarGoogle Scholar |
Sakudo A, Toyokawa Y, Misawa T, Imanishi Y (2017) Degradation and detoxification of aflatoxin B1 using nitrogen gas plasma generated by a static induction thyristor as a pulsed power supply. Food Control 73, 619–626.
| Degradation and detoxification of aflatoxin B1 using nitrogen gas plasma generated by a static induction thyristor as a pulsed power supply.Crossref | GoogleScholarGoogle Scholar |
Scally L, Lalor J, Gulan M, Cullen PJ, Milosavljević V (2018) Spectroscopic study of excited molecular nitrogen generation due to interactions of metastable noble gas atoms. Plasma Processes and Polymers 15, e1800018
| Spectroscopic study of excited molecular nitrogen generation due to interactions of metastable noble gas atoms.Crossref | GoogleScholarGoogle Scholar |
Schmidt M, Zannini E, Arendt EK (2018) Recent advances in physical post-harvest treatments for shelf-life extension of cereal crops. Foods 7, 45–66.
| Recent advances in physical post-harvest treatments for shelf-life extension of cereal crops.Crossref | GoogleScholarGoogle Scholar |
Scholtz V, Pazlarova J, Souskova H, Khun J, Julak J (2015) Nonthermal plasma – a tool for decontamination and disinfection. Biotechnology Advances 33, 1108–1119.
| Nonthermal plasma – a tool for decontamination and disinfection.Crossref | GoogleScholarGoogle Scholar | 25595663PubMed |
Selcuk M, Oksuz L, Basaran P (2008) Decontamination of grains and legumes infected with Aspergillus spp. and Penicillum spp. by cold plasma treatment. Bioresource Technology 99, 5104–5109.
| Decontamination of grains and legumes infected with Aspergillus spp. and Penicillum spp. by cold plasma treatment.Crossref | GoogleScholarGoogle Scholar | 17993274PubMed |
Shahrzad Mohammadi S, Dorranian D, Tirgari S, Shojaee M (2015) The effect of non-thermal plasma to control of stored product pests and changes in some characters of wheat materials. Journal of Biodiversity and Environmental Sciences 7, 150–156.
Shi H, Ileleji K, Stroshine RL, Keener K, Jensen JL (2017a) Reduction of aflatoxin in corn by high voltage atmospheric cold plasma. Food and Bioprocess Technology 10, 1042–1052.
| Reduction of aflatoxin in corn by high voltage atmospheric cold plasma.Crossref | GoogleScholarGoogle Scholar |
Shi H, Cooper B, Stroshine RL, Ileleji KE, Keener KM (2017b) Structures of degradation products and degradation pathways of aflatoxin B1 by high-voltage atmospheric cold plasma (HVACP) treatment. Journal of Agricultural and Food Chemistry 65, 6222–6230.
| Structures of degradation products and degradation pathways of aflatoxin B1 by high-voltage atmospheric cold plasma (HVACP) treatment.Crossref | GoogleScholarGoogle Scholar | 28643515PubMed |
Siciliano I, Spadaro D, Prelle A, Vallauri D, Cavallero MC, Garibaldi A, Gullino ML (2016) Use of cold atmospheric plasma to detoxify hazelnuts from aflatoxins. Toxins 8, 125–134.
| Use of cold atmospheric plasma to detoxify hazelnuts from aflatoxins.Crossref | GoogleScholarGoogle Scholar |
Siddique SS, Hardy GESJ, Bayliss KL (2018) Cold plasma: a potential new method to manage postharvest diseases caused by fungal plant pathogens. Plant Pathology 67, 1011–1021.
| Cold plasma: a potential new method to manage postharvest diseases caused by fungal plant pathogens.Crossref | GoogleScholarGoogle Scholar |
Ten Bosch L, Pfohl K, Avramidis G, Wieneke S, Viol W, Karlovsky P (2017) Plasma-based degradation of mycotoxins produced by Fusarium, Aspergillus and Alternaria species. Toxins 9, 97–108.
| Plasma-based degradation of mycotoxins produced by Fusarium, Aspergillus and Alternaria species.Crossref | GoogleScholarGoogle Scholar |
Walter GH, Chandrasekaran S, Collins PJ, Jagadeesan R, Mohankumar S, Alagusundaram K, Ebert PR, Daglish GJ, Nayak MK, Mohan S, Srivastava C, Chadda IC, Rajagopal A, Reid R, Subramanian S (2016) The grand challenge of food security – general lessons from a comprehensive approach to protecting stored grain from insect pests in Australia and India. Journal of Grain Storage Research 78, 7–16.
| The grand challenge of food security – general lessons from a comprehensive approach to protecting stored grain from insect pests in Australia and India.Crossref | GoogleScholarGoogle Scholar |
Warrick C (2013) ‘Cooling or drying for quality control. Aerating stored grain – a grains industry guide.’ (Ed. C Nicholls) (Grain Research & Development Corporation: Canberra, ACT) Available at: https://www.graintec.com.au/media/34545/Aerating%20stored%20grain%20-%20A%20Grains%20Industry%20Guide.pdf (accessed 30 July 2020).
Ziuzina D, Misra N, Cullen P, Keener KM, Mosnier J, Vilaró I, Gaston E, Bourke P (2016) Demonstrating the potential of industrial scale in-package atmospheric cold plasma for decontamination of cherry tomatoes. Plasma Medicine 6, 397–412.
| Demonstrating the potential of industrial scale in-package atmospheric cold plasma for decontamination of cherry tomatoes.Crossref | GoogleScholarGoogle Scholar |