Impact of plasma processed air (PPA) on phenolic model systems: Suggested mechanisms and relevance for food applications
Introduction
Recently, cold atmospheric pressure plasma (CAPP) technology has attracted extensive attention among food scientists and has evolved to be a promising technique with great potential for application to food. The direct, semi-direct or indirect application of plasma is of interest in the food sector as it can be used to treat food at temperatures below 70 °C (Schlüter et al., 2013). The combination of its nonthermal character with its ability to operate at atmospheric pressure makes CAPP a suitable approach for the treatment of heat-sensitive products.
Whereas the penetration depth of plasma-immanent species is limited during treatment of solids, in liquid foods, however, it is supported by convection and in this case most of the bulk comes into contact with the applied plasma or at least with the subsequent reaction products. This implicates that all components contained may react with plasma-immanent species, and are thereby affected. Due to their interaction with water and other molecules, plasma reactive oxygen (ROS) and nitrogen (RNS) species initiate several chain reactions, resulting in a large variety of different reactive molecular entities. Dependent on the plasma source and the process parameters, most important ROS substance class formed in liquids are hydroxyl radicals (OH), which are able to react and form hydrogen peroxide (H2O2). Depending on the pH value, the latter can be very stable and remain active in the liquid far beyond the plasma exposure time. In addition, hydroperoxy radicals (OOH−) or superoxides (O22−) can be formed in the presence of OH radicals, which can also be quite stable (Ikawa et al., 2010; Zhang et al., 2006).
Using a microwave driven plasma discharge and air as the process gas to produce plasma processed air (PPA), longer-living RNS come into contact with the matrix to be treated. Composed of 78.08% nitrogen, 20.95% oxygen, and 0.97% argon, Bacri and Raffanel (1987) calculated that exposure of standardized air to a plasma source induces the formation of 28 species (including electrons) contained in the excited plasma state and divided the plasma-specific species into eight families: atomic nitrogen (N, N+, N+++, N+++), dinitrogen (N2, N2+), nitric oxide (NO, NO+, NO−), nitrogen dioxide (NO2, NO2+, NO2−), nitrous oxide (N2O, N2O+, N2O−) atomic oxygen (O, O+, O++, O+++, O−), dioxygen (O2, O2+. O2−), and argon (Ar, Ar+, Ar2+, Ar3+). These species are not stable and depending on the treatment conditions recombine to more stable reaction products. By treating liquids with dry plasma gas, many chemical reactions can take place in the gas phase, the liquid phase and at the interface. The main resulting products could be NO−, NO2−, NO3−, O2−, O- and N2O3 in the gas phase, HO−, HNO2 and HNO3 in the gas and liquid phase and H2O2, ONOOH, HNO2 and HNO3 in the liquid phase (Schnabel et al., 2015).
PPA generated by a microwave-driven plasma torch has been applied to successfully inactivate enzymes (Bußler et al., 2017), as well as microorganisms (Baier et al., 2013) and bacterial spores (Hertwig et al., 2015a) on the surfaces of fresh and dry food (Baier et al., 2014; Baier et al., 2015a), spices and herbs (Hertwig et al., 2015b) and meat (Fröhling et al., 2012). Results obtained in studies reporting PPA specific browning reactions in fruits and vegetables notwithstanding enzyme inactivation indicate that oxidation and polymerization reactions of secondary plant metabolites as phenolic compounds occur as a result of PPA treatment under certain process conditions (Bußler et al., 2017).
Since phenolic compounds as one group of antioxidants contained in fresh plant food matrices determine the path of reaction cascades initiated by ROS and RNS, these substances are of particular importance with regard to the occurring molecular radical interactions between plasma-immanent species and molecules themselves as well as consequent reactions of the subsequently formed intermediates. Phenolic compounds are secondary metabolites formed via the shikimate pathway in higher plants and microorganisms as well as via pentose phosphate pathway by phenylpropanoid metabolism (Randhir et al., 2004). They contain benzene rings substituted with one or more hydroxyl substituents and vary from simple phenol molecules to highly polymerized compounds (Velderrain-Rodríguez et al., 2014). Plant polyphenols have gained considerable interest as dietary antioxidants based on active reports of their alleged contribution to the containment of a variety of human diseases (Fiorentino et al., 2008; Hoper & Cassidy, 2006; Pu et al., 2013). Fruits, vegetables and beverages are the main sources of phenolic compounds in human nutrition.
Excitation of nitrite or nitrate ions in PPA may induce oxidation, nitration, nitrosation or di-/polymerization of phenolic derivatives at the liquid-gas interface. These reactions result from the direct excitation of aromatic compounds in the presence of nitrate ions (Suzuki et al., 1982), the plasma-immanent species or the excitation of nitrate ions formed in the liquid (Jones et al., 2000; Mulvaney et al., 1998). Due to the fact, that specific antioxidants are commonly found in fruits, vegetables, grains and sugar beets frequently used in beverage applications, it is very likely that the formation of phenolic plasma reaction products occur during plasma treatment of liquid media as juices or smoothies or in cells injured by the cutting of fresh cut products.
In this context, the purpose of this study was to investigate the effects of PPA on different food related phenolic compounds in aqueous model solutions. Chlorogenic and caffeic acid were selected on basis of previous work on fresh sliced apples and potatoes (Bußler et al., 2017). The fact that in case of PPA treatment of apple but not for potato a browning reaction was observed was the main reason for taking into account chlorogenic acid as the main phenolic compound in these products. In the same context, caffeic acid was selected, since it represents the phenolic part of the chlorogenic acid molecule. Further, pyrocatechol was included, as it has been used as standard compound in many studies representing a simple phenolic moiety containing two hydroxyl groups in ortho-position allowing the formation of o-quinone by oxidation, which in turn leads to formation of browning pigments. The study further aims to specify the reaction products and investigates antioxidant capacity, pH value and UV–Vis spectra as exemplary markers providing information on the changes caused by the PPA treatment. Special emphasis was set on developing methods for separation and identification of reaction products based on reverse phase high performance liquid chromatography (RP-HPLC) and liquid chromatography/mass spectrometry (LC-MS) in order to gain first insights into the occurring reaction mechanisms of identified plasma-specific reaction products.
Section snippets
Sample preparation
Three model food compounds served as test material: pyrocatechol (benzene-1,2-diol, Carl Roth, Karlsruhe, Germany), chlorogenic acid ((1S,3R,4R,5R)-3-[(E)-3-(3,4 dihydroxyphenyl)prop-2-enoyl]oxy-1,4,5-trihy-droxycyclohexane-1-carboxylic acid, Sigma Aldrich, Steinheim, Germany) and caffeic acid ((E)-3-(3,4-dihydroxyphenyl)prop-2-enoic acid, Sigma Aldrich, Steinheim, Germany). The hydroxycinnimic acid derivates used were dissolved in distilled water and each diluted to a final concentration of
Accumulation of nitrate, nitrite and hydrogen peroxide in pure water
The results obtained in this study demonstrate the accumulation of nitrate and nitrite in pure water induced by treatment with PPA for up to 10 min (Fig. 1, left and center). The concentration of hydrogen peroxide was in the range of 4 to 6 mg L−1 in treated and control samples (Fig. 1, right). The nitrate concentration increased strongly from 10 to 1084 mg L−1 upon exposure to PPA for 1 min. Prolonging the treatment time to 10 min decreased it to a final concentration of about 880 mg L−1.
Conclusion
Results of this study provide evidence for the PPA-induced formation of oxidized, nitrated and polymerized phenolic compounds for all three focal model substances. The results clearly indicate that the plasma-induced reactions, as well as the formation and degradation of reactants are dependent on the process duration. However, further experiments and analyses are necessary to clarify their chemical composition. Underlying reaction mechanism could not be fully elucidated and need to be
Author agreement statement
We the undersigned declare that this manuscript is original, has not been published before and is not currently being considered for publication elsewhere.
We confirm that the manuscript has been read and approved by all named authors and that there are no other persons who satisfied the criteria for authorship but are not listed. We further confirm that the order of authors listed in the manuscript has been approved by all of us.
We understand that the Corresponding Author is the sole contact
Declaration of competing interest
All authors concur with the submission, the work in its present form has not been submitted to a scientific journal before, and there is no commercial conflict of interest.
Acknowledgements
We gratefully acknowledge the technical assistance of Arved Jeltsch (University of Potsdam) and the scientific support of Jörg Ehlbeck in plasma application (Leibniz Institute for Plasma Science and Technology).
This work was partially supported by the competence cluster “NutriAct-Competence Cluster Nutrition Research Berlin-Potsdam” funded by the Federal Ministry of Education and Research (Grant No. 01EA1408A-G), by the project “Plasma-based decontamination of dried plant related products for
References (62)
- et al.
Laccase-catalyzed poly(ethylene glycol)-templated ‘zip’ polymerization of caffeic acid for functionalization of wool fabrics
Journal of Cleaner Production
(2018) - et al.
Direct non-thermal plasma treatment for the sanitation of fresh corn salad leaves: Evaluation of physical and physiological effects and antimicrobial efficacy
Postharvest Biology and Technology
(2013) - et al.
Non-thermal atmospheric pressure plasma: Screening for gentle process conditions and antibacterial efficiency on perishable fresh produce
Innovative Food Science and Emerging Technologies
(2014) - et al.
Impact of plasma processed air (PPA) on quality parameters of fresh produce
Postharvest Biology and Technology
(2015) - et al.
Effect of atmospheric pressure cold plasma (APCP) on the inactivation of Escherichia coli in fresh produce
Food Control
(2013) - et al.
Pre-drying treatment of plant related tissues using plasma processed air: Impact on enzyme activity and quality attributes of cut apple and potato
Innovative Food Science & Emerging Technologies
(2017) - et al.
Photooxidative degradation of 4-nitrophenol (4-NP) in UV/H2O2 process: Influence of operational parameters and reaction mechanism
Journal of Hazardous Materials
(2007) - et al.
Indirect plasma treatment of fresh pork: Decontamination efficiency and effects on quality attributes
Innovative Food Science & Emerging Technologies
(2012) - et al.
Impact of remote plasma treatment on natural microbial load and quality parameters of selected herbs and spices
Journal of Food Engineering
(2015) - et al.
Decontamination of whole black pepper using different cold atmospheric pressure plasma applications
Food Control
(2015)
Kinetic study of the oxidation and nitration of catechols in the presence of nitrous acid ionization equilibria
Journal of Hazardous Materials
Photochemically induced nitration and hydroxylation of organic aromatic compounds in the presence of nitrate or nitrite in ice
Journal of Photochemistry and Photobiology A: Chemistry
Apples increase nitric oxide production by human saliva at the acidic pH of the stomach: A new biological function for polyphenols with a catechol group?
Free Radical Biology and Medicine
Stimulation of phenolics, antioxidant and antimicrobial activities in dark germinated mung bean sprouts in response to peptide and phytochemical elicitors
Process Biochemistry
Dietary polyphenols generate nitric oxide from nitrite in the stomach and induce smooth muscle relaxation
Toxicology
Effect of added citrus fibre and spice essential oils on quality characteristics and shelf-life of mortadella
Meat Science
Calculation of some thermodynamic properties of air plasmas: Internal partition functions, plasma composition, and thermodynamic functions
Plasma Chemistry and Plasma Processing
Theoretical foundations of radiation chemistry
Positive corona inception voltages and corona currents for air at various pressures and humidities
Dielectrics and Electrical Insulation, IEEE Transactions on
Interactions with aqueous solutions of the air corona products
Revue de Physique Appliquée
A REVIEW tailing of survival curves of bacterial spores
Journal of Applied Bacteriology
Aerobic coupling of aqueous phenols catalyzed by binuclear copper: Ring substituent effect and the kinetics of the coupling of o-methylphenol
American Institute of Chemical Engineers Journal
Characterization of 2-S-glutathionylcaftaric acid and its hydrolysis in relation to grape wines
Journal of Agricultural and Food Chemistry
Nonenzymic autoxidative phenolic browning reactions in a caffeic acid model system
Journal of Agricultural and Food Chemistry
Caffeic acid autoxidation and the effects of thiols
Journal of Agricultural and Food Chemistry
Characterization of the products of nonenzymic autoxidative phenolic reactions in a caffeic acid model system
Journal of Agricultural and Food Chemistry
Preliminary investigation of prebreakdown phenomena and chemical reactions using a pulsed high-voltage discharge in water
Industry Applications, IEEE Transactions on
The effect of UV absorption on the photocatalytic oxidation of 2-nitrophenol and 4-nitrophenol
Journal of Applied Electrochemistry
Stimulation of acidic reduction of nitrite to nitric oxide by soybean phenolics: Possible relevance to gastrointestinal host defense
Journal of Agricultural and Food Chemistry
Isolation and structure elucidation of antioxidant polyphenols from quince (Cydonia vulgaris) peels
Journal of Agricultural and Food Chemistry 2008
Cited by (4)
Principles of non-thermal plasma processing and its equipment
2022, Non-thermal Food Processing Operations: Unit Operations and Processing Equipment in the Food IndustryPilot-scale generation of plasma processed air and its influence on microbial count, microbial diversity, and selected quality parameters of dried herbs
2022, Innovative Food Science and Emerging TechnologiesCitation Excerpt :However, specific toxicological aspects have to be assessed firstly on pilot-scale to evaluate the industrial relevance. Phenolic compounds have shown reactions after plasma treatment into nitr(os)ated products, which have to be examined for a possible human endangerment (Bußler, Rawel, & Schlüter, 2020). Plasma induced browning effects on apple pieces could be possibly also attributed to these nitration or polymerization reactions (Bußler, Ehlbeck, & Schlüter, 2017).
Nonthermal Processing Technologies for Stabilization and Enhancement of Bioactive Compounds in Foods
2022, Food Engineering ReviewsEfficiency of plasma-processed air for biological decontamination of crop seeds on the premise of unimpaired seed germination
2021, Plasma Processes and Polymers