Effect of non-thermal plasma technology on microbial inactivation and total phenolic content of a model liquid food system and black pepper grains
Graphical abstract
Introduction
Dried food ingredients including grains, spices and powders have low water activities which limitsmicrobial growth. However, pathogenic and spoilage microorganisms and spores have been found in several dried foods. For example, a Salmonella outbreak associated with the consumption of ready-to-eat salami products containing contaminated black pepper was reported in the United States (Gieraltowski, Julian, Pringle, Macdonald, Quilliam, Marsden-Haug et al., 2013). Contamination events generally occur because of poor hygiene practices during cultivation, harvesting and food manufacturing. A significant number of microorganisms are associated with dried food ingredients, pathogens of particular significance include Salmonella spp, Bacillus spp and Clostridium perfringens. In response to adverse environmental conditions, the later two of these microorganisms may produce dormant structures or bacterial spores, which are resistant to many treatments. Conventional technologies for decontamination of dried ingredients include super-heated steam, fumigation with ethylene or propylene oxide and ionizing radiation. However, there are many limitations associated with use of these technologies including nutrient degradation, health risks, legislative obstacles and consumers’ concerns. Indeed, ethylene and propylene oxide have been banned in the European Union because of carcinogenic and mutagenic concerns (Fowles, Mitchell, & McGrath, 2001; Regulation, 2008). Even though gamma-rays and x-rays have been shown to have strong potential to improve food safety with limited impacts on quality, consumers continue to have a negative perception of food irradiation treatments (Bearth & Siegrist, 2019). Additionally, conventional thermal treatments e.g. super-heated steam affect food quality due to the high processing temperatures involved. These limitations have encouraged researchers to investigate alternative approaches to ensure safety of dried food ingredients.
Plasma is defined as a partially or wholly ionized gas composed of positive and negative ions, electrons, photons, free radicals and neutrons atoms and molecules (Fridman & Kennedy, 2004). The ionization of these chemically reactive components can occur upon exposure to different energy sources, the most common being thermal, microwave and radio frequency, radioactive (gamma radiation) and x-ray electromagnetic radiation. Depending on its thermodynamic equilibrium state, plasma can be classified as thermal or non-thermal. Unlike thermal plasma treatments, the electrons and other gas components comprising cold plasma exist in a non-thermodynamic equilibrium (Shashi K Pankaj & Keener, 2017). Cold plasma has traditionally been used in the bio-medical, textile and polymer industries (Fanelli & Fracassi, 2017; Kim, Kim, Hong, & Yang, 2010; Sun & Stylios, 2004). However in the last decade it has been increasingly investigated as an alternative approach to the use of conventional technologies in the food industry. Advantages of cold plasma compared to traditional technologies include: extension of product shelf life with limited impacts of food quality, higher retention of the nutrients in the food matrix, and reduced environmental impacts due to lower energy, water and solvent requirements (Hati, Patel, & Yadav, n.d.; Shashi K; Pankaj, Wan, & Keener, 2018). Applications of cold plasma technology in the food industry investigated to date include inactivation of microorganisms in food products (Dasan, Yildirim, & Boyaci, 2018; Misra & Jo, 2017; Pasquali, Stratakos, Koidis, Berardinelli, Cevoli, Ragni, et al., 2016), modification of functional properties of food matrices (Bahrami et al., 2016; Kovačević et al., 2016; Thirumdas, Saragapani, Ajinkya, Deshmukh, & Annapure, 2016), improvement of food packaging (Oh, Roh, & Min, 2016; Shashi Kishor; Pankaj, Bueno-Ferrer, Misra, Milosavljević, O'Donnell, Bourke, et al., 2014) and hydrogenation of edible oils (Yepez & Keener, 2016). Adaptive plasma sources and designs employed these applications include: dielectric barrier discharges, corona discharge, gliding arc discharges, radio frequency, microwave and jet plasma (Ekezie, Sun, & Cheng, 2017). The energetic species generated by plasma can alter and inactivate microorganisms (Misra, Tiwari, Raghavarao, & Cullen, 2011). This study investigates the effects of a non-thermal atmospheric pressure plasma jet on microbial inactivation in an innoculated model liquid food system and black pepper grains, and on the total phenolic content of black pepper grains.
Section snippets
Dried ingredients
Black pepper grains (Piper nigrum L.) were purchased from a commercial supplier (Brand Heera, P&B Ltd, West Yorkshire, United Kingdom).
Microbial growth and inoculation
Two matrices were used, namely a model liquid food system inoculated with Bacillus subtilis vegetative cells, and black pepper grains inoculated with B subtilis vegetative cells and spores. B subtilis DSM 618 (Merck KGaA, Germany) was grown in nutrient broth for 24 h at 30 °C under shaking conditions (150 rpm). Black pepper grains were inoculated with the
Microbial inactivation
Fig. 2a–c shows the vegetative cells population (log CFU/mL) in an innoculated model liquid food system and black pepper for 15 kV and 30 kV for treatment times of 3 and 5 min respectively after storage for 1h (Figs. 2a), 24 h (Fig 2b) and 48 h (Fig. 2c) post treatment at 4 °C. Significant differences (p < 0.05) were observed for all samples after storage for 24 h compared to control or 1 h post treatment. For 3 min of treatment at 15 kV, the microbial loads of the model liquid food system was
Conclusion
Cold plasma technology was demonstrated to have to be more effective for a model liquid food system compared to black pepper grains contaminated with vegetative cells, with 4.65 ± 0.70 log reduction compared to 2.40 ± 0.70 log reduction for samples treated at 30 kV for 5 min and stored for 24 h at 4 °C. The SEM images showed distinguishable changes in cells' morphology after plasma treatment. Plasma treatment reduced the smoothness of the cell membrane due to lesions, eventually leading to cell
Declaration of competing interest
Declarations of interest for the manuscript “EFFECT OF NON-THERMAL PLASMA TECHNOLOGY ON MICROBIAL INACTIVATION AND TOTAL PHENOLIC CONTENT OF MODEL LIQUID FOOD AND BLACK PEPPER GRAINS” submitted to Lebensmittel-Wissenschaft & Technologie - Food Science & Technology Journal: none.
Acknowledgements
This research was carried out with the financial support of the Irish Department of Agriculture, Food and the Marine, project no 14F845.
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