The effects of hydrogen incorporation in modified atmosphere packaging on the formation of biogenic amines in cold stored rainbow trout and horse mackerel
Graphical Abstract
Introduction
Fish is considered an extremely perishable product due to its high nutritional value and delicate chemical structure. The growth of spoilage microorganisms is considered the primary reason behind the formation of biogenic amines (BAs) in fish (Gram and Dalgaard, 2002, Houicher et al., 2021). BAs are mostly generated through the decarboxylation of free amino acids upon microbial activity. The main BAs formed in fish products are histamine, putrescine, cadaverine, tyramine, tryptamine, 2-phenylethylamine, spermine, and spermidine (Ozogul, 2009).
Production of BAs in food products forms a serious challenge for food producers, logistic chains, retailers, and researchers. Although limited tools are available to protect food products from the risk of BA formation, there are a few potential strategies for achieving this goal: 1- decreasing the growth of proteolytic microorganisms, 2- decreasing the expression or activity of proteolytic enzymes, 3- increasing the catabolism of amino acids, 4- decreasing the growth of decarboxylase-producing microorganisms, 5- decreasing the expression or activity of decarboxylases, 6- increasing the growth of microorganisms with the ability to oxidise amines, and 7- increasing the expression or activity of amine oxidases.
A modified atmosphere packaging (MAP) has been reported to retard the formation of BAs to some extent in fish commodities by decreasing the growth of decarboxylase-producing microorganisms (Qian et al., 2018). MAP has been shown to extend the shelf life of fish products by up to two folds depending on the initial quality and the processing practices (Kocatepe et al., 2010). Undesirable chemical and enzymatic reactions along with microbial growth are prevented by restricting O2 and increasing CO2 in MAP (Emborg et al., 2002). Qian et al. (2018) investigated the effect of active substances (quercetin, cinnamic acid, and 4 hexylresorcinol) in combination with MAP (80% CO2/10% N2/10% O2) on the formation of BAs in the Pacific white shrimp (Qian et al., 2018). They found that MAP decreased psychrotrophic bacteria counts and reduced the level of most BAs. In another study, Del Nobile et al. (2009) reported that combining thymol (110 mg/kg) with MAP in three different gas formulations could inhibit the formation of BAs in fresh bluefish burgers for 28 days at 4 °C of storage, whereas MAP was not able to prevent microbial spoilage alone (Del Nobile et al., 2009). .
Molecular hydrogen (H2) is a colorless and tasteless gas that is classified as a food additive with the code of E949. In the EU, it is detailed in part C (Group I) of regulation 1129/2011; food additives are permitted in all categories of foods at quantum satis (Bulut et al., 2022). The detonation and flammability limits of H2 in the air are 18.3–59% and 4–75% (v/v), respectively, which makes the use of H2 safe under the conditions applied in the present study; i.e. at levels as low as 4% (v/v). Hydrogen possesses several benefits when it is considered for health and food applications, which can be attributed to the known selective antioxidant, anti-radical, anti-inflammatory, anti-apoptosis, anti-stress, and anti-cancer properties of H2 (Alwazeer et al., 2021; Cachon and Alwazeer, 2019). The use of hydrogen as a reducing agent is proposed to conserve the quality of different foods such as fresh white cheese (Alwazeer et al., 2020), dairy beverages enriched with polyunsaturated fatty acids (Giroux et al., 2008), pasteurized orange juice (Alwazeer et al., 2003), and strawberries (Alwazeer and Özkan, 2022).
Oxidoreduction potential (ORP, Eh) is an electrochemical parameter expressing the capacity of a compound to gain or lose electrons (Martin et al., 2013). By decreasing the ORP of a medium to negative values, i.e. low ORP, using a reducing agent such as hydrogen gas, for example, oxidation reactions are limited as the abundance of free electrons available for biochemical reactions effectively neutralises oxidative compounds such as the highly deleterious hydroxyl radical (.OH) (Alwazeer, 2020). In addition, molecular hydrogen incorporation has been reported to selectively reduce oxygen radicals, thereby limiting lipid oxidation (rancidity) within cells and the subsequent growth of aerobic microorganisms (Martin et al., 2013). To illustrate, low-ORP (reducing conditions) are more favorable in degrading amino acids, i.e. phenylalanine (Phe), leucine (Leu), and methionine (Met) than high-ORP (oxidative conditions) in Lactococcus lactis NCDO763 (Kieronczyk et al., 2006). Low-ORP of the medium, controlled by reducing compounds such as hydrogen gas, has been found to modify the catabolic activities of some microorganisms by increasing the enzymatic activity, or expression of such enzymes as lactate dehydrogenase (LDH) and formate dehydrogenase in Escherichia coli (Riondet et al., 2000a), and biosynthesis and activity of hydroperoxide lyase in Yarrowia lipolytica (Husson et al., 2006, Riondet et al., 2000b). Levels of lactate dehydrogenase (LDH) and alcohol dehydrogenase (ADH) in Leuconostoc mesenteroides were found to be 2-fold higher under the hydrogen gas atmosphere compared with that of nitrogen one (Bourel et al., 2003). Reducing conditions have been reported to induce a 7-fold increase in levels of NADPH-dependent hypothetical oxidoreductase (Zhu et al., 2014).
Some lactic acid bacteria (LAB) strains isolated from fish pastes have been found to produce one or more BAs (Dapkevicius et al., 2000). Several studies have revealed that reducing conditions are not favorable for the growth of microorganisms such as LAB. Ouvry and co-workers demonstrated that the growth of Lactobacillus plantarum can be slowed, whilst the acidification process may also be delayed under reducing conditions controlled by hydrogen gas (Ouvry et al., 2002). Additionally, reducing conditions were also unfavorable for the growth of E. coli (George et al., 1998, Riondet et al., 1999). Furthermore, the lag phase of Leuconostoc mesenteroides was shown to be 6 times longer under reducing conditions, (again controlled by hydrogen gas) than that of the oxidizing ones, controlled by nitrogen gas (Bourel et al., 2003). It has been reported that each microbial species optimally grows within a certain ORP range, and a modification of extracellular ORP can lead to a change in an organism's metabolic flux (Zhu et al., 2014). The modality of low-ORP on decreasing microbial growth is as yet unknown (Zhu et al., 2014). Reports evidence that enzymes involved in biomass constituent synthesis and F0F1 ATPase components were under-expressed in low-ORP conditions. The increase in microbial membrane permeability under low-ORP conditions was found to be related to the action of low-ORP on membrane proteins of the cell (Riondet et al., 1999). Cytoplasmic ORP can also be altered by the addition of reducing compounds into a medium, leading to a favorable modification of the oxidoreductive state of protein thiols and/or charged amino acids (Gill et al., 1998).
On the other hand, the ethanol extracts of some spices have exhibited high inhibition activity against amino acid decarboxylases (ADs) such as histidine, lysine, and ornithine decarboxylases (Wendakoon and Sakaguchi, 1995). The subsequent enzyme inhibition effect has been explained by the delay in amine formation by E. aerogenes. Such inhibition of enzymatic activity has been correlated with the antioxidant activity (reducing capacity) of phenolic compounds found in alcohol-based extracts. Of pertinence here is that a relationship between the antioxidant activity of extracts and their low-ORP value has been revealed (Alwazeer and Dham, 2019). The inhibition effect of phenolic plant extracts has been also correlated with the hydrophobic character of phenols and their ability to partition lipids and disrupt the structure of the cellular membrane. Thus, these phenolics can alter the membrane's permeability leading to leakage of cell contents and ions (Özogul et al., 2015). A similar effect can also be obtained when hydrogen gas is used for lowering the ORP of the bacterial growth medium (Riondet et al., 1999). For example, low-ORP conditions were shown to de-energize E. coli by increasing membrane permeability and sensitivity to protons through modification of the thiol:disulfide balance within protein structures (Gill et al., 1998). From contemporary literature reports, it can be hypothesized that the low-ORP environment produced by molecular hydrogen may affect the growth of decarboxylase-producing microorganisms in food products such as fish. In a previous study, the presence of molecular hydrogen in washing water significantly decreased the formation of BAs in butter (Bulut et al., 2022). The present study aims to evaluate the impact of incorporating molecular hydrogen into a modified atmosphere packaging (called Reducing Atmosphere Packaging, RAP) on the formation of BAs in rainbow trout and horse mackerel during cold storage.
Section snippets
Preparation of fish samples
Whole fish of rainbow trout (Oncorhynchus mykiss) and horse mackerel (Trachurus trachurus) were caught from the Euphrates River and the Black Sea, respectively. All fish samples were immediately brought to the laboratory under ice and washed with cold tap water, beheaded, and eviscerated. Approximately 500 g of samples were packaged in polyethylene laminated polystyrene plates (Çokay Plastik, Turkey) with a covering polyethylene film (100 µm thickness) (Çokay Plastik, Turkey) using a
Method validation
The coefficient of determination showed good linearity of data in the calibration curve. The coefficient of determination (R2) for all BA standards ranged between 0.995 and 0.999. The LODs of the method for all standards were found to be in the range of 0.6–4.3 ng/mL. The LOQs of the method for all standards were found to be in the range of 1.7–12.9 ng/mL (Table 1).
Biogenic amine formation
Fig. 1, Fig. 2, Fig. 3, Fig. 4, Fig. 5, Fig. 6 show the progress in the levels of histamine, tyramine, putrescine,
Conclusion
Limiting the formation of BAs requires the optimization of fish handling and processing protocols. The modified atmosphere packaging proposed for this purpose showed limited potential. In this study, the incorporation of molecular hydrogen in the conventional MAP showed a potent ability to restrict the formation of BAs in both freshwater and seawater fish species, i.e., rainbow trout and horse mackerel, respectively, during cold storage. Reduction rates of BAs were about two folds in RAPs
CRediT authorship contribution statement
Yasemin Çelebi Sezer: Methodology, Investigation, Writing – original draft. Menekşe Bulut: Methodology, Investigation. Gökhan Boran: Conceptualization, Validation, Reviewing, Project administration. Duried Alwazeer: Supervision, Conceptualization, Writing – review & editing.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This study was supported by the Iğdır University Scientific Research Projects Coordinatorship in Turkey (Project number, MÜF0820A23).
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