A critical analysis of the cold plasma induced lipid oxidation in foods

Accepted Manuscript A critical analysis of the cold plasma induced lipid oxidation in foods Mohsen Gavahian, Yan-Hwa Chu, Amin Mousavi Khaneghah, Francisco J. Barba, N.N. Misra PII:

S0924-2244(18)30143-2

DOI:

10.1016/j.tifs.2018.04.009

Reference:

TIFS 2212

To appear in:

Trends in Food Science & Technology

Received Date: 1 March 2018 Revised Date:

22 April 2018

Accepted Date: 25 April 2018

Please cite this article as: Gavahian, M., Chu, Y.-H., Khaneghah, A.M., Barba, F.J., Misra, N.N., A critical analysis of the cold plasma induced lipid oxidation in foods, Trends in Food Science & Technology (2018), doi: 10.1016/j.tifs.2018.04.009. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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A critical analysis of the cold plasma induced lipid oxidation in foods

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Mohsen Gavahiana*, Yan-Hwa Chu a, Amin Mousavi Khaneghah b, Francisco J. Barbac, N. N. Misrad

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Product and Process Research Center, Food Industry Research and Development Institute, No. 331 Shih-Pin Rd., Hsinchu, 30062, Taiwan, ROC

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Department of Food Science, Faculty of Food Engineering, University of Campinas (UNICAMP), Campinas, São Paulo, Brazil

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Universitat de València, Faculty of Pharmacy, Preventive Medicine and Public Health, Food Science, Toxicology and Forensic Medicine Department, Nutrition and Food Science Area, Avda.Vicent Andrés Estellés, s/n, 46100 Burjassot, València, Spain Research and Development, General Mills India Pvt Ltd, Mumbai 79, India

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* Corresponding author: [email protected]; [email protected]

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Abstract

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Background: Cold plasma is an emerging, economical and environment-friendly technology with potential applications in food and bioprocessing industry, including microbial decontamination, enzyme inactivation, shelf-life extension, and physicochemical modification. These advantages stem from the cocktail of reactive species and the physical processes that are associated with gaseous electrical discharges. However, when oxygen is present as a component of the gas in which plasma discharges are made, the reactive oxygen species (ROS) could result in decreased food quality. The lipids oxidation induced by an oxygen-containing cold plasma process can eventually affect the acceptability and shelf-life of foods.

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Scope and approach: Product safety and quality are crucial considerations for the industrial adoption of cold plasma technology, necessitating a comprehensive review. This review critically analyses the oxidative impact of this novel technology on lipids, highlights the practical implications, and proposes strategies to mitigate the challenges.

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Key findings and conclusions: Cold plasma in oxygen-containing inducer gases affects the lipids in several food materials including cereals, edible oils, dairy, and meat products. Therefore, it is necessary to understand and address its oxidative effects in different foods. Processing the appropriate food types under optimized process conditions along with the careful handling of the plasma-treated foods are among the key considerations to minimize the negative impacts on food lipids.

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Keywords: Emerging technologies; Lipid oxidation; Non-thermal plasma; Food quality; Food safety.

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1. Introduction

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Industrial need for higher production rates and quality improvement along with consumers’ food diversity demand are among the driving forces for traditional process improvements and process development. The emerging food technologies aim to improve the food safety and extend shelf-life, while maximizing the retention of key quality attributes (Misra, et al., 2017). Cold plasma is relatively a new and emerging technology in agri-food processing sector and widely attracting the interest of food industry owing to its economic and environmental-friendly traits (Pankaj, Wan, & Keener, 2018).

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Plasma is an ensemble of several excited atomic, molecular, ionic, and radical species, co-existing with numerous reactive species, including electrons, positive and negative ions, free radicals, gas atoms, molecules in the ground or excited state, quanta of electromagnetic radiation (UV photons and visible light) (Misra, et al., 2017). It is these active chemical species of cold plasma that are capable of rapidly and effectively inactivating micro-organisms in their native environments or result in functional changes in foods, thus attracting the industry. Cold plasma has been demonstrated to have potential applications in an array of operations, including: microbial decontamination (Dasan, Boyaci, & Mutlu, 2017; McClurkin-Moore, Ileleji, & Keener, 2017; Noriega, Shama, Laca, Diaz, & Kong, 2011), physicochemical modification of starch (Wu, Sun, & Chau, 2017; Zhu, 2017), proteins (Bußler, Steins, Ehlbeck, & Schlüter, 2015; Dong, Gao, Zhao, Li, & Chen, 2017) and cereal products (Misra, et al., 2015; Pal, et al., 2016) as well as pesticide degradation in foods (Misra, 2015; Toyokawa, Yagyu, Yamashiro, Ninomiya, & Sakudo, 2018). However, with every opportunity there often come many challenges. Cold plasma is also reported to promote oxidative processes in some food systems, which needs to be carefully addressed, and this forms the topic of the present review.

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While lipid molecules have an important role in food palatability and nutrition, their oxidation adversely affects the sensory and nutritional quality (Barden & Decker, 2016; Shahidi & Zhong, 2010). The oxidized lipids have toxic effects on cellular processes, including modulation of the gene expression, alteration of cell behavior, and cardiovascular diseases (Niki, 2009; Spickett & Forman, 2015). The traditional processes such as conventional thermal treatments and their effects on food characteristics are exhaustively-understood, thanks to the efforts of researchers for several decades. However, with the on-going development of non-thermal technologies, a good understanding of their effects on critical safety and quality parameters is a prerequisite for their commercialization. This holds true even for cold plasma induced lipid oxidation in foods. It should be noted that notwithstanding the reported adverse effects on lipids, researchers are actively continuing to explore its uses and designing novel plasma sources for food applications.

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In one of the earliest review of cold plasma applications for food safety, the need for

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ACCEPTED MANUSCRIPT investigation of the effects of plasma on the fate of lipids was strongly emphasized (Misra, Tiwari, Raghavarao, & Cullen, 2011). It was expressed that such information is important for a thorough scientific understanding and practical commercial adoption of the technology as a decontamination intervention. Since then, few studies have evaluated the effects of cold plasma on lipids isolated from the complex matrix. However, much progress has been made in investigating the effects of cold plasma on lipids in real food systems. This review analyses the progress made in this direction, as evidenced by the research conducted over the past six years. For completeness, the review provides a succinct description of the cold plasma technology and the chemical aspects of importance to oxidative changes in foods. Towards the end of the review, some strategies to mitigate the lipid oxidation in plasma treated foods and possible applications of plasma induced oxidation are also outlined.

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2. Chemistry of cold plasma

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Cold plasma can be obtained at atmospheric or sub-atmospheric pressures by means of an electric discharge or strong ultraviolet radiation in a gas. The corona discharge, dielectric barrier discharge (DBD), radio-frequency plasma, microwave plasma, plasma jets and the gliding arc discharge are among the plasma sources commonly employed for direct or indirect treatment of food materials (Fridman, 2008; Misra, Schlüter, & Cullen, 2016). The detailed designs of several plasma sources are amply discussed in the literature (Bárdos & Baránková, 2010; Conrads & Schmidt, 2000). The plasma properties, such as the number density of charged particles (electrons and ions) and their energy distribution, generally depend on the power intensity, a power source (e.g. AC, DC, pulsed, frequency, etc.), gas type etc. A good introduction to the physics, chemistry and technological details of cold plasma sources can be found in a recent book by Misra, Schlüter, et al. (2016). Therefore, we will confine our review to a discussion of the chemistry of cold plasma in oxygen or gas mixtures containing oxygen as a component.

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Electric fields in gases can accelerate the motion of the charged ions and free electrons. The collisions of these accelerated particles with other molecules result in energy sharing, displacement reactions, and charge exchanges, resulting in the formation of several radical species. In particular, the reaction mechanisms involve electronic impact processes (vibration, excitation, dissociation, attachment, and ionization), ion-ion neutralization, ion-molecule reactions, Penning ionization, quenching, three-body neutral recombination, and neutral chemistry, besides photoemission, photo-absorption and photo-ionization (Misra, Pankaj, Segat, & Ishikawa, 2016). It should be noted that while most of the species formed in the plasma treatment can interact with foods, a large fraction of the species also recombine or diffuse into the liquid phase.

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When electrical discharges are made in feed gases containing N2 and O2 molecules,

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ACCEPTED MANUSCRIPT their collision reactions with electrons result in a cascade of reactions to form NxOy, O3 (ozone), and peroxy- radicals. In a discharge, the collision of electrons (e-) with molecular O2 results in a lone O atom within the discharge zone, which subsequently attacks molecular O2 by a three-body reaction to yield ozone (O3)- a powerful oxidant: + +

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where, M = O, O2, or O3. The ozone and singlet oxygen are some of the key agents responsible for the antimicrobial action of plasma and despite anything contrary, potential sources of oxidation of lipids in foods. Water, when present in the feed gas, results in the formation of OH, H2O2 and H species, which in turn may potentially subdue the O3 molecules.

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3. Lipid oxidation

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Lipids are constituted of fatty acids- saturated, monounsaturated or polyunsaturated, basis the number of double bonds between the carbons. Food lipids are prone to the oxidation process in the presence of catalytic systems such as light, heat, and metals (e.g. Cu, Fe) which involve free radicals or other intermediate reactive species and result in photo-, thermal- or auto-oxidation. The latter is the most common pathway of oxidation, defined as the spontaneous reaction of food lipids with oxygen through the chain reactions of free radicals which involve three distinct stages of initiation, propagation, and termination (see Fig. 1) (Lorenzo, et al., 2017). Free radicals, which can be produced by several processes attack several compounds such as unsaturated fatty acids and result in lipid oxidation, ultimately negatively impact the food quality (Frankel, 2012; Kerrihard, Pegg, Sarkar, & Craft, 2015; Repetto, Semprine, & Boveris, 2012; Shahidi & Zhong, 2010). Several analytical methods can detect the incidence of lipid oxidation in foods by measuring the primary oxidation products (which are usually non-volatile components) or the secondary oxidation products (which often comprise volatile components) as in peroxide value (PV) and 2-thiobarbituric acid reactive substances (TBARS) assays, respectively (Kerrihard, et al., 2015). Besides, advanced techniques such as chromatography, Fourier-transform infrared spectroscopy (FTIR) and nuclear magnetic resonance spectroscopy (NMR) may also be employed to evaluate lipid oxidation (Frankel, 2012; Repetto, et al., 2012).

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The ROS from plasma could interact with food lipids and initiate the oxidation process, especially when treating fatty foods (Van Durme & Vandamme, 2016). The primary targets of ROS (particularly OH• and 1O2) in lipid moieties are methyl groups, with greater affinity for those linked by double bonds. This is due to the fact that the energy needed for abstraction of a hydrogen atom is significantly lower than CHbonds linked elsewhere (272 kJ/mol vs. 422 kJ/mol) (Surowsky, Bußler, & Schlüter,

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ACCEPTED MANUSCRIPT 2016). Thus, the more double bonds a fatty acid contains, the more susceptible it is against homolytic ROS attacks. Lipids, being quite sensitive components of food matrices, their fate needs to be monitored during plasma treatment processes. Typical ROS sensitive fatty acids are e. g. Linoleic acid (18:2) and α-Linolenic acid (18:3), containing two and three double bonds, respectively. In practice too, it was reported that a 20-minute cold plasma treatment altered the polyunsaturated fatty acids compositions and the total aldehyde content of cow milk which could be related to the hydrolytic effects of plasma (Korachi, et al., 2015). While sufficient attention has been provided to structural and physical changes during cold plasma process, lipid oxidation has not received the attention it deserves.

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4. Cold plasma induced lipid oxidation in foods

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4.1. Effects of cold plasma treatment on food lipid oxidation

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Plasma process generates reactive oxygen species such as hydroxyl radicals, hydrogen peroxide, and superoxide anions that participate in microbial decontamination (Attri, et al., 2015). Unfortunately, the reactive species (particularly the free radicals) can also initiate the lipid oxidation process by abstracting hydrogen ions from lipid molecules (Shahidi & Zhong, 2010). Several investigations reported the oxidative impact of cold plasma on food ingredients. This emerging technique negatively affected the fatty acids of rice (Lee, et al., 2017), wheat flour (Bahrami, et al., 2016), pork (Choi, Puligundla, & Mok, 2015; Cui, Wu, Li, & Lin, 2017; Jayasena, et al., 2015; Kim, et al., 2011; Kim, Yong, Park, Choe, & Jo, 2013; Lee, et al., 2018), beef (Bauer, et al., 2017; Jayasena, et al., 2015; Rød, Hansen, Leipold, & Knøchel, 2012; Sarangapani, Ryan Keogh, Dunne, Bourke, & Cullen, 2017), chicken (Lee, et al., 2016), seafood (Albertos, Martin-Diana, Cullen, Tiwari, Ojha, Bourke, Alvarez, et al., 2017; Choi, Puligundla, & Mok, 2016; Choi, Puligundla, & Mok, 2017a, 2017b; Puligundla, Choi, & Mok, 2017), sushi (Kulawik, et al., 2018), cheese (Yong, Kim, Park, Alahakoon, et al., 2015), milk (Kim, et al., 2015) and olive oil (Van Durme & Vandamme, 2016). A summary of the recent studies investigating the oxidative effects of cold plasma in food systems is provided in Table 1 and forms the basis for further discussion in the sections that follow.

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4.2. Cereals

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In general, cereal grains have low lipid content and plasma treatment is unlikely to cause significant oxidation for rapid treatments. However, there are exceptions with cereals rich in lipids (such as oats, chia), when the bran is included, or when a fraction of the cereal is processed. In a study by Lee, et al. (2017), atmospheric 6

ACCEPTED MANUSCRIPT pressure plasma treatment (250 W) was found to cause undesirable oxidative effects in white and brown rice. The authors reported that 20 minutes exposure to cold plasma increased the TBARS values of the white and brown rice from 0.04 and 0.49 to 0.25 and 0.59, respectively. Firstly, the TBARS value of plasma treated brown rice was higher than that of white rice (0.59 vs. 0.25) suggesting that cold plasma might be more suitable for the food with limited fat content. Secondly, the oxidative effect of cold plasma increased when increasing the processing time (Lee, et al., 2017). The oxidation effect in this case, is likely due to the long processing times and the highpower density. Bahrami, et al. (2016) applied atmospheric pressure cold plasma on the wheat flour and observed an increase in oxidation markers over longer exposure time. They also reported that increasing the applied voltage increased the abundance of oxidative markers. The study concluded that plasma process optimization is necessary for treating a product with high lipid content such as whole flour. As such, for fine particulate materials, the high surface area provides ample sites for attack by oxidative species. Therefore, the suitability of the type of cereal, the gas mixture, power density, and treatment time could be important levers for optimizing the flour treatment processes.

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4.3. Red meat and poultry

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4.3.1. Pork

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Unlike that for cereals, ample research has been conducted to evaluate oxidative effects of cold plasma during treatment of pork. A 100 W atmospheric pressure plasma treatment for 1.5 minutes has been found to enhance the microbiological safety of bacon but with negative effects on the fat observed as an increase in the TBARS value after 7 days of storage (Kim, et al., 2011). However, no increase in TBARS value was observed on the same day of the plasma treatment. It should be noted that generation of ROS, their reaction with food lipids and formation of TBARS, as a by-product of lipid peroxidation, is not an instantaneous reaction. Therefore, low TBARS value recorded immediately after plasma treatment should not be used for concluding that plasma has no negative impact on food lipids. The fluctuating TBARS results over the storage time of plasma treated pork (Kim, et al., 2011) revealed that long-term monitoring of this oxidation marker can provide a better estimate of the quality of plasma treated commodities. Kim, et al. (2013) reported that although plasma process of pork loin reduced the population of Escherichia coli and Listeria monocytogenes, lipid oxidation occurred, thereby deteriorating the sensory quality (i.e., odor) and the overall acceptability of the final product. The study revealed that the presence of oxygen in the carrier gas mixture enhanced the oxidation rate. The authors suggested that further investigations on elucidating quality changes of plasma treated samples are required. Fresh pork was also affected by cold plasma and experienced lipid oxidation. A two-min 20 kV corona discharge plasma jet treatment at 1.5 A reduced the microbial population (Escherichia coli and Listeria monocytogenes) of the fresh and frozen pork surfaces without

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The effect of a 60 min atmospheric plasma treatment on the physiochemical properties of a pork-based batter was investigated by Jung, et al. (2017) and no sign of lipid oxidation was observed in the plasma treated batter according to the malondialdehyde concentrations of the samples. The study concluded that different plasma treatment systems might affect food lipids differently and; therefore, selecting suitable equipment and defining appropriate process conditions can protect the food lipid from oxidation during plasma treatment. Similarly, exposure to a 600 W cold plasma did not increase the malondialdehyde content of canned ground hams (Lee, et al., 2018). The lipid oxidation in the studied product was prevented by the available antioxidants in the studied meat batters, i.e., nitric oxide and ascorbic acid (Lee, et al., 2018; Repetto, et al., 2012). The ascorbic acid molecule can donate an electron and stabilize radicals and together with nitric acid, they exhibit antioxidant activity and bind oxygen, iron ions, and free fatty-acids (Honikel, 2008; Nimse & Pal, 2015). Therefore, the availability of antioxidants in a food system can increase the oxidative stability and protect lipids from the cold plasma generated reactive species. Likewise, Cui, et al. (2017) investigated the effects of cold nitrogen plasma on the pork lipid and reported that plasma treatment significantly increased the TBARS value of the plasma-treated meat. However, incorporating antioxidant components such as butylated hydroxyanisole (BHA) and lemongrass essential oils compensated the oxidative effect of plasma and; therefore, oxidation markers of the antioxidant-enriched pork following a two-min cold plasma treatment did not change. In addition to the protection against oxidation, the synergistic antibacterial activity of cold plasma and lemongrass essential oils was reported in pork loin (Cui, et al., 2017).

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The findings of Jayasena, et al. (2015) highlighted the importance of plasma process duration on lipid oxidation. Short-term plasma treatment by a flexible thin-layer DBD did not affect or slightly affected the pork lipids within a conductive package by an as in the case of 2.5 and 5 minute treatment times, respectively. However, following a 10 minute exposure of pork meat to plasma, TBARS values increased by about 30% (from 0.3 to 0.4 mg malondialdehyde/kg) and consequently, the taste preference (sensory score) of the pork-butt was decreased (Jayasena, et al., 2015). According to the literature, TBARS values of 0.5-2.0 mg are the detectable organoleptic threshold of off-flavor in meat products (Gray, Gomaa, & Buckley, 1996).

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Applying atmospheric pressure cold plasma for one minute at the power of 62 W to Bresaola (dried and aged salted beef) inside a modified atmosphere package (30% O2 and 70% Ar) adversely affected the beef lipids and increased the TBARS value from 0.15 to about 0.35 mg/kg (Rød, et al., 2012). Similar values of TBARS was reported by Jayasena, et al. (2015) for a 10-min plasma treated beef loin. According to the reported data by Rød, et al. (2012), lipid oxidation correlates with increasing the input power (from 15.5 to 31 W), plasma exposure time (from two seconds to one minute) and storage time (1-14 days) (Rød, et al., 2012). Similarly, Sarangapani, et al. (2017) reported that plasma treated beef was free from oxidation products when the exposure time was limited to less than half an hour. However, long exposure time to plasma oxidized the beef lipids. The same conclusion has been drawn for beef loins wherein short process times did not cause lipid oxidation while extended plasma treatment did result in oxidation (Jayasena, et al., 2015). Therefore, the plasma process parameters such as exposure time could be optimized to reduce the lipid oxidation of the plasma-treated products.

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It was reported that direct exposure of beef loins to high power atmospheric pressure air plasma (discharge power of 0.7 W/cm2) reduced microbial surface count without oxidizing the beef lipid after 10 days of storage (Bauer, et al., 2017). It should be noted that these meats were vacuum packaged after plasma treatment and the oxygen was excluded from sample surrounding area. Therefore, an appropriate packaging system following the plasma treatment can retain the sensory quality of food by preventing it from further oxidation.

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4.3.3. Chicken

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Exposure to the flexible thin-layer DBD (100 W peak power and 2 W average power) for 10 minutes did not affect the oxidation markers of the packaged chicken breast. However, this process successfully reduced the population of Listeria monocytogenes, Escherichia coli, Salmonella Typhimurium and total aerobic bacteria by 2.1-3.4 Log CFU/g (Lee, et al., 2016). The findings of Lee, et al. (2016) showed that the chicken breast is more stable to plasma oxidative effect than red meat. This could be related to the difference between the fat content of these meats as the oxidation products concentration can be increased by increasing the fat content of the food materials. The fat content of chicken breast is lower than many parts of red meats such as pork butt. Furthermore, TBARS value is correlated with the concentration of ferric heme pigment and myoglobin which are more abundant in red meat as compared to chicken breast (Lee, et al., 2016; Love & Pearson, 1971; Rhee, Anderson, & Sams, 1996). Therefore, the oxidative impact of plasma treatment on the chicken breast was confirmed to be less than that of red meat.

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4.4. Seafood

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Five-min exposure to cold plasma induced lipid oxidation in the Hosomaki and Nigiri sushi products and the TBARS of Hosomaki sushi was higher than that of Nigiri samples (Kulawik, et al., 2018). A higher surface area along with the presence of the high concentration of unsaturated fatty acid in the formulation made the Hosomaki more sensitive to the oxidation process (Dawczynski, Schubert, & Jahreis, 2007; Kulawik, et al., 2018). Similarly, corona discharge jet enhanced the sanitary quality of semi-dried squid but caused lipid oxidation. As a result, the TBARS value of plasma treated samples were found to increase during storage (Choi, et al., 2017b). The authors mentioned that lipid oxidation during plasma treatment could be related to the further reaction of the primary lipid oxidation products with reactive species generated by the jet plasma. They also observed that the drying process produced primary lipid oxidation products such as free fatty acids which made the squid's lipid more prone to oxidation induced by cold plasma treatment. Moreover, the susceptibility of squid to oxidation could be related to its fat composition. This seafood contains large amounts of unsaturated fatty acids which are more vulnerable to oxidation than saturated ones (Jong Hwan, Heesun, Sang Hyun, Jeong Hwa, & Jae Cherl, 2007). Jet plasma under ambient condition produces several reactive species including ozone, singlet oxygen, and peroxide which might influence the squid lipids. Therefore, the nature of the food material and the way that product is handles before plasma exposure can affect the oxidation rate in plasma treatment. Similar results were reported for corona discharge jet treatment of dried squid shreds, and the authors proposed that the increase in TBARS value during the plasma treatment could be related to the unsaturated fatty acids oxidation and the partial dehydration of the dried squids. The paper concluded that vacuum packaging of the plasma-treated squid might prevent oxidative rancidity (Choi, et al., 2017a). Likewise, TBARS values of dried Alaska Pollock shreds and Gwamegi (semi-dried Pacific saury) increased following a corona plasma jet treatment (Choi, et al., 2016; Puligundla, et al., 2017). In the same manner, atmospheric cold plasma generated by an in-package DBD reduced the population of the spoilage bacteria (total aerobic psychrotrophic, Pseudomonas and lactic acid bacteria) but oxidized the lipids of fresh mackerel (Scomber scombrus) fillets. Also, comparison of applied voltages (70 kV and 80 kV) and exposure time (1, 3 and 5 min) revealed that an increase in these variables resulted in higher oxidation rate (Albertos, Martin-Diana, Cullen, Tiwari, Ojha, Bourke, & Rico, 2017). Therefore, process parameter optimization can reduce the rate of lipid oxidation in plasma treatment. According to the publications mentioned above, it seems that lipid oxidation could be a crucial concern while treating seafood with plasma due to the presence of a high concentration of polyunsaturated fatty acid in this product.

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4.5. Milk and dairy products

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Sarangapani, et al. (2017) detected the secondary oxidation products in the milk fat (butter oil) only after an extended plasma process times (i.e., half an hour) at high a voltage (80 kV). According to their report, the input energy and process time influence the rate of lipid oxidation in oily foods. In addition, they proposed that the lipid oxidation under cold plasma treatment obey the Criegee mechanism, i.e., direct attack of ozone to produce ozonide (see Fig. 2). Their investigations on chemical analyses by chromatography, infrared spectroscopy, NMR revealed that the typical oxidation products of a plasma treated food are ozonides, aldehydes (hexanal, pentanal, nonanal and nonenal), carboxylic acids (9-oxononanoic, octanoic and nonanoic acid), and hydroperoxides (9and 13-hydroperoxyoctadecadienoylglycerol).

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Ten- minute exposure of milk to encapsulated DBD plasma (250 W power) was sufficient to reduce the Listeria monocytogenes, Escherichia coli and Salmonella typhimurium counts by 2.4 log CFU/mL without any significant sign of lipid oxidation (Kim, et al., 2015). In contrast to the findings of Kim, et al. (2015), the TBARS values of cheddar cheese increased when plasma treatment (peak power of 100 W for 10 min) was employed to reduce the population of the same microorganisms up to 6 log CFU/g (Yong, Kim, Park, Alahakoon, et al., 2015). The fat content of cheddar cheese is higher than raw milk. In addition, the plasma equipment and condition were different in the two above mentioned research. Therefore, the TBARS values vary depending on the plasma type, working gas and characteristics of the plasma-treated sample, such as fat content and fatty acid composition. In addition, according to Yong, Kim, Park, Kim, et al. (2015), plasma treatment time is also a determining factor for lipid oxidation as the TBARS value of cheddar cheese increased by 30% following a 7.5 min additional plasma treatment, i.e. from 0.14 ± 0.02 to 0.18 ± 0.03 for 2.5 and 10 min exposure time, respectively.

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5. Considerations to minimize the lipid oxidation

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It is evident from our discussion in section 4 that several process parameters influence lipid oxidation during plasma treatment. Careful selection of the parameters can help food processors to decrease the incidence and/or degree of lipid oxidation in the plasma treated food. Choosing the appropriate raw material and formulation along with plasma treatment under an optimized condition are among the critical considerations to retain the lipid quality in cold plasma processing of food.

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5.1. Selective processing of foods

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It is clear that plasma treatment (with oxygen in feed gas) of high-fat content foods such as edible oils increases the chance of oxidation product incidence. It was

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ACCEPTED MANUSCRIPT reported that longer exposure of olive oil to the plasma produced a high concentration of secondary oxidation products (Van Durme & Vandamme, 2016). Obviously, plasma treatment of a lipid matrix should be avoided. Chicken breast has lower fat content than beef and pork which makes it a potential candidate for cold plasma treatment from the viewpoint of minimization of lipid oxidation (Jayasena, et al., 2015; Lee, et al., 2016). A similar conclusion could be made for dairy products such as cheddar cheese (fat content of 17-30%), which is susceptive to the oxidation during plasma processes as compared to cow’s milk with a fat content between 1.43.2% (Guinee, Auty, & Fenelon, 2000; Kim, et al., 2015; Yong, Kim, Park, Kim, et al., 2015).

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In addition to the fat content, the composition of the food lipid should be taken into account. For example, a high concentration of unsaturated fatty acids renders the squid in the danger of oxidation when subjected to plasma treatment, considering its richness in unsaturated fats (Choi, et al., 2017a, 2017b). In the same way, as the concentrations of polyunsaturated fatty acids in sunflower oil is higher than virgin olive oil, plasma treatment of the former oil was found to result in a higher oxidation rate (Van Durme & Vandamme, 2016).

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Non-fat components of food can also affect the oxidation rate in plasma treatment, depending on their pro- or antioxidant properties such as in case of ferric heme and ascorbic acid, respectively. As pointed out earlier, the presence of ferric heme pigment and myoglobin in a product such as red meat enhanced the oxidation rate under the plasma condition as compared to that of poultry (Lee, et al., 2016; Love & Pearson, 1971; Rhee, et al., 1996). Therefore, poultry is likely a better candidate for industrial plasma processing than red meat with due considerations to lipid oxidation (Lee et al., 2016).

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Finally, the way food is handled prior to plasma treatment, including storage conditions and any pre-processing should be given due consideration. Poor storage conditions such as exposure to oxygen and light (Frankel, 2012; Shahidi & Zhong, 2010) and harsh processes such as drying (Jong Hwan, et al., 2007) initiate the oxidation process and make the lipids more prone to the plasma induced oxidative condition. To illustrate this, plasma treatment of squids prior to drying has been reported to enhance the production of the primary oxidation products, making the lipids more vulnerable to oxidation during storage (Choi, et al., 2017a, 2017b).

422

5.2. Optimizing the product formulation

423 424 425 426 427

Food lipids are susceptible to oxidation in the presence of reactive species which are inherent to any plasma process. Therefore, preventive measures against oxidative reactions could be considered while plasma processing sensitive foods (i.e., foods with high-fat content or high concentration of unsaturated fatty acids). Addition of the approved food additives with antioxidant properties such as BHA or the natural

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ACCEPTED MANUSCRIPT antioxidant compounds such as essential oils could protect the food product from oxidation during plasma treatment. To demonstrate this concept, Cui et al., 2017 mixed pork meat with BHA and cymbopogon (lemongrass) essential oils thereby preventing the oxidation from cold plasma species. Natural phenolics with antioxidant properties added to foods prior to plasma treatment may synergize and protect the endogenous antioxidants. It should be noted that essential oils and their ionized products, per se are antimicrobial, thus they synergistically improve the antimicrobial efficacy of cold plasma (Tyagi, Malik, Gottardi, & Guerzoni, 2012). It is also worthwhile mentioning that several essential oils enjoy generally recognized as safe (GRAS) status by the U.S. food and drug administration (U. S. Food and drug administration, 21CFR182.20).

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5.3. Handling the plasma treated food

440 441 442 443 444 445 446

The availability of oxygen and light as well as elevated temperatures increase the lipid oxidation rate and therefore, excluding oxygen and light as well as storing the final product at appropriate conditions can delay the onset of oxidation (Frankel, 2012). It was reported that vacuum packaging of plasma-treated beef postponed the oxidation over a period of 10-days (Bauer, et al., 2017). Likewise, Choi, et al. (2017b) suggested that vacuum packaging of plasma treated squids could considerably limit the oxidation during storage.

447

5.4. Optimizing process parameters

448 449 450 451 452 453 454 455 456

Plasma treatment under non-optimal conditions, such as excessive input energy, long processing times, elevated temperatures and improper working gas renders the product more susceptible to lipid oxidation. Therefore, plasma treatment at the minimum possible input power, for the shortest possible duration, controlling the process temperature and if applicable, excluding oxygen from the working gas mixture, could significantly improve the quality of the final product. However, a comprehensive study for each product is necessary to find the optimum plasma process conditions which can effectively decontaminate the food or enhance the functional properties, while retaining the quality and sensory attributes.

457

6. Cold plasma for accelerated oxidative stability testing

458 459 460 461 462 463 464 465

While lipid oxidation is undesirable in many food systems, the ability of cold plasma in enhancing the oxidation rate in the presence of oxygen has been leveraged as a tool for accelerated lipid oxidation to simulate traditional slow stability testing methods (Van Durme & Vandamme, 2016; Vandamme, et al., 2015). The traditional methods of accelerated lipid oxidation rely on elevated temperatures to associate with chemical reactions and consequently, the results of these methods and long terms natural oxidation at ambient condition differ considerably (Krichene, et al., 2010). Van Durme, Nikiforov, Vandamme, Leys, and De Winne (2014) compared the

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ACCEPTED MANUSCRIPT oxidation rate of vegetable oils with cold plasma vis-à-vis thermally-based reference assay. They reported that plasma treatment at room temperature for a short time formed the volatile components that were also observed in naturally deteriorated vegetable oil after a long storage time. They concluded that cold plasma could be employed to investigate the role of individual reactive species and speed up lipid oxidation at low temperatures.

472 473 474 475 476 477 478 479 480 481 482 483 484 485 486 487 488

Vandamme, et al. (2015) accelerated the oxidation of fish oil via cold plasma and detected the typical lipid oxidation markers in the plasma treated fish oil, although these compounds were not the same as the ones in the naturally aged sample. This research group also proposed cold plasma as a tool to predict the antioxidant activity of alpha-tocopherol in the fish oil. Both the investigations mentioned above concluded that plasma treatment has the potential to turn into a tool for realistically accelerating lipid oxidation. However, cold plasma process needs to be optimized to predict lipid oxidation more precisely. For this purpose, the effects of cold plasma condition on the oxidation rate of oleic acid were studied. The correlation between plasma-oxidized and naturally aged oleic acid was found to be 82% following the optimization of the plasma process. The authors concluded that by increasing the oxygen concentration of the carrier gas and the applied voltage, as well as reducing the moisture content and the distance between nozzle and sample surface, the oxidation rate of olive oil was enhanced (Vandamme, et al., 2016). A snapshot of the experimental details and salient results of the relevant research studies is provided in Table 2. In conclusion, cold plasma could potentially replace the rancimat testing protocol used for lipid stability.

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[Table 2 about here]

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7. Conclusions

491 492 493 494 495 496 497 498 499 500 501 502 503

When applying a novel technology as cold plasma, chemical changes in food components, particularly lipids, need careful consideration for industrial adoption. Literature reveals that cold plasma could induce lipid oxidation in an array of foods, including rice, wheat flour, pork, beef, chicken, seafood, cheese, milk and vegetable oils via the action of reactive species. Effective plasma treatment of high-fat foods is invariably a challenging task and demands optimization of product and process parameters. The presence of pro-oxidant components in foods subjected to cold plasma and inappropriate storage conditions can render the food lipids more vulnerable to oxidation. Adjusting product formulation (such as minimizing the fat content, reducing the concentration of unsaturated fatty acids and incorporating antioxidants), applying plasma at lower power ranges for shorter times, as well as eliminating oxygen during and/or after plasma treatment are among some important strategies to overcome the challenge of lipid oxidation.

504

Elucidating the impact of cold plasma parameters on lipid oxidation in foods and

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ACCEPTED MANUSCRIPT optimizing the underlying factors is a key prerequisite for industrial adoption of this emerging technology. The strategies outlined in our review could help mitigate the challenges associated with plasma treatment of foods, without placing significant economic or technological barriers. It is our opinion that at present, intensive research to assess the up-scaling potential of plasma processes in the food industry is more important for future success.

511 512 513 514 515 516 517 518

The oxidation of food lipids due to plasma species, though a challenge for most known applications, also presents opportunities for the industry. Cold plasma induced rapid and controlled oxidation can be developed as an analysis tool for accelerated lipid oxidation studies. Furthermore, the reactive species led rapid oxidation of effluent streams rich in fatty substances, e.g. from edible oil processing, dairy and meat industry is yet another opportunity with huge potential. In fact, research for cashing on plasma technology as an advanced oxidation process for industrial effluent treatment is underway.

519

Acknowledgments

520 521

This research work was supported by the Ministry of Economic Affairs, project no. 106-EC-17-A-22-0332, Taiwan, Republic of China.

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Table 1. Summary of the investigations on the effect of cold plasma on food lipid oxidation.

Pork butt and beef loin

Bacon

He, 10 lpm He + 10 sccm O2

Sliced cheddar cheese

Oxidation assay

Key findings

Reference

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TBARS

Plasma treatment increased the TBARS values of brown and white rice The TBARS value of brown rice was higher than that of white rice due to higher fat content Lipid oxidation during plasma process affected the sensory characteristics

Lee et al., 2017

Air

2

- PV - nhexanal

The oxidation markers increased by increasing process time and applied voltage

Bahrami et al. 2016

Air+N2+O2

10

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Air

TBARS

The TBARS values of treated pork and beef samples increased with process time The TBARS values of beef-loin samples were higher than those of pork-butt because of the variations in fat content and fatty-acid composition

Jayasena et al., 2015

1. 5

TBARS

Higher TBARS values in treated samples after 7 days of storage was observed

Kim et al., 2011

He, 99.7%He + 0.3%O2

10

TBARS

TBARS values of He+O2-treated samples were greater than those of other samples

Kim et al., 2013

Air + N2 + O2

10

TBARS

The TBARS values increased compared to those of the non-treated samples

Yong et al., 2015

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Pork loin

Direct exposure, APP; Powers: 75, 100, 125 W Frequency: 14 MHz Indirect exposure, DBD plasma; Power: 3 kV; Frequency: 30 kHz Indirect exposure; Flexible thinlayer DBD plasma; Peak power: 100 W; average power: 2W; Frequency: 15 kHz

Process time*

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Wheat flour

Carrier gas

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Brown and white cooked rice

Plasma source and condition Direct exposure; atmospheric pressure; Power: 250 W; Frequency: 15 kHz Direct exposure; NTP, Input power: 40, 90 W; Frequency: 9 kHz Indirect exposure; Flexible thinlayer DBD plasma; peak power: 100 W; average power: 2 W; Frequency: 15 kHz

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ACCEPTED MANUSCRIPT Indirect exposure, Inpackage APP plasma-DBD system; Voltage: 60– 80 kV

Air

Milk

Direct exposure, Encapsulated DBD plasma; Power: 250 W; Frequency: 15 kHz Indirect exposure; DBD; Power: 62 W; Frequency: 27.8 kHz

Air

Air

2

TBARS

TBARS value was not affected by plasma treatment

Kim et al., 2015

The TBARS values increased with plasma power, treatment time and storage time

Rød et al., 2012

SC

1

Sarangapa ni et al., 2017

- PV - TBARS

Air

Corona jet treatment increased the PV of frozen pork but did not affect unfrozen pork lipid TBARS levels did not change upon a plasma treatment

Choi et al., 2015

3

TBARS

The TBARS levels of corona plasma jet treated squid increased with increasing exposure time

Choi et al., 2017a

Air

5

Plasma treatment modified the fatty acids composition Increasing the input voltage and process time increased the oxidation rate

Albertos et al., 2017

Air

10

- Fatty acid compositi on - PV -Dienes - TBARS TBARS

Plasma treatment did not cause lipid oxidation

Lee et al., 2016

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Dried squid shreds

Direct exposure; corona discharge; Voltage: 20 kV; Frequency: 58 kHz; current strength: 1.50 A; span: 25 mm Direct exposure; corona discharge; Input voltage: 20 kV; Frequency: 58 kHz; current strength: 1.50 A; span: 25 mm Indirect exposure; DBD plasma; frequency: 50 Hz; Voltage: 70, 80 kV Indirect exposure; Flexible thinlayer DBD plasma; Peak power: 100 W; Average

70% N2 + 30% O2

Cold plasma increased the PV of both dairy and beef fat The formation of hydroperoxides of oleic and linoleic acid was observed Oxidation of cold plasma treated fatty acids follow the Criegee mechanism.

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Pork

- PV - NMR Spectroscop y -FTIR -Fatty acid composition 10 TBARS

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Bresaol a (a sliced readyto-eat meat)

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Beef and dairy lipids

Fresh macker el fillets

Chicken breast

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ACCEPTED MANUSCRIPT power: 2 W Frequency: 15 kHz

Sushi (Nigiri and Hosom aki)

Vacuum package d beef loin

- PV - TBARS

PV was unaltered during the corona treatment but TBARS increased

99.9% Ar + 0.1% O2

60

GC-MS

Durme and Vandamm e, 2016

Air

5

Plasma treatment increased the concentration of secondary oxidation products plasma- induced oxidation followed a unique mechanism yielding unique oxidation products Cold plasma was proposed as a technique to evaluate edible oil adulteration Plasma treatment increased the TBARS content of sushi samples Higher surface area and higher concentration of unsaturated fatty acids resulted in higher levels of TBARS in Hosomaki sushi

Air

1

TBARS value was not affected by plasma process

Bauer et al., 2017

SC

TBARS

TBARS

Air

Gwame gi (Semidried Pacific Saury) Semidried squid

Kulawik et al., 2018

60

TBARS

Cold plasma did not cause lipid oxidation in meat batter Cold plasma process conditions can protect the food lipid from oxidation

Jung et al., 2017

Air

30

TBARS

Cold plasma did not induce lipid oxidation Antioxidants (nitric oxide and ascorbic acid) prevented the product from oxidation upon cold plasma treatment

Lee et al., 2018

Air

10

- PV - TBARS - Acid value

The PV and acid value were not affected by corona treatment but TBARS increased

Puligundla et al., 2017

Air

10

TBARS

TBARS levels of the corona jet treated samples increased.

Choi et al., 2017b

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Canned ground ham

Choi et al., 2016

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Meat batter

Air

M AN U

Olive oil

Direct exposure; corona discharge; Voltage: 20 kV; Frequency: 58 kHz; Current strength: 1.50 A; Span: 25 mm Direct exposure; DBD plasma jet; Input voltage: 6KV; Frequency: 50 kHz Direct exposure; DBD based jet; Voltage: 70 and 80 kV; Frequency: 50 Hz. Direct exposure; APP system; Dissipated power: 18, 22, 25 W Direct exposure; DBD plasma; Power: 550 W; Frequency: 25 kHz Direct exposure; DBD; Power 600 W; Frequency: 25 kHz Direct exposure; corona jet; Voltage: 20 kV; frequency: 58 kHz Direct exposure; corona jet; Voltage: 20 kV;

TE D

Dried Alaska Pollock Shreds

22

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2

TBARS

Cui et al., 2017

* The maximum plasma exposure time (minutes) to the plasma in the study.

716

Table 2- Studies investigating cold plasma as an accelerated lipid oxidation technique. Plasma process condition Radio-frequency plasma jet treatment; Frequency: 14 MHz; Power: 25 W

Fish oil

Frequency: 50 KHz; Voltage: 60 kV; Current: 128 mA; Exposure time: 60 min

Oleic acid

Voltage: 0-15 kV Frequency: 50 KHz

Working gas Ar, Ar + O2 (00.6%), Ar+H2O (0-0.6%)

Van Durme et al., 2014.

Cold plasma treatment yielded several lipid oxidation products which were also found in the naturally aged fish oil Cold plasma successfully predicted the antioxidant effect of alpha-tocopherol on fish oil

Vandamme et al., 2015.

The most promising result was observed for Ar+O2 gas High correlation was observed between plasma treated sample and naturally oxidized sample at ambient temperature

Vandamme et al., 2016.

EP

Ar+O2, Ar+H2O

Reference

Plasma treatment with Ar gas did not induce lipid oxidation but short treatment with both O2 + Ar and H2O + Ar plasmas yielded several oxidation products Cold plasma showed the potential of being an accelerated lipid oxidation technique. Ability to control the type or concentration of reactive species, non-thermal character and short process time are the key benefits of cold plasma as an accelerated lipid aging tool

TE D

Ar+O2 (0.6%)

Key findings

M AN U

Evaluated sample Commercial blended vegetable oil

AC C

717

TBARS value increased by cold plasma treatment Addition of antioxidants (BHA, essential oils) reduced the amount of TBARS and compensated the oxidative effects of cold plasma

SC

715

N2

RI PT

Pork loin

Frequency: 58 kHz; Current strength: 1.5 A; Span: 25 mm Indirect exposure; a commercial cold N2 plasma; Power: 500 W

23

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Figures

M AN U

SC

RI PT

718

719

AC C

EP

721

Fig. 1- The lipid autoxidation pathway

TE D

720

722

24

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Fig. 2. The mechanisms of plasma induced oxidation for oleic acid (Sarangapani, Ryan Keogh, Dunne, Bourke, & Cullen, 2017; it has been reproduced with permission, Order Number: 4334051258770)

AC C

EP

TE D

M AN U

SC

RI PT

726

25

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Highlights When unchecked, the reactive species in plasma could promote lipid oxidation. Processing of selected foods under optimized conditions is recommended.

RI PT

Intelligent product reformulation enables suppressing plasma induced oxidation. Reducing the input power, process time and temperature is recommended.

AC C

EP

TE D

M AN U

SC

Accelerated lipid oxidation via plasma can be leveraged for rapid stability testing.