Vegetable extracts: Effective inhibitors of heterocyclic aromatic amines and advanced glycation end products in roasted Mackerel
Introduction
Adding two servings a week of fatty fish to human daily menu are recommended by dietitians and health professionals owing to various benefits for brain and heart health (Kiefer, 2003). Mackerel, as a super-nutritious food, almost bursting with protein, unsaturated fatty acid and high in essential vitamins and minerals, which appear on people’s tables as the most common fish (Singer et al., 1986). Thermal processing of mackerel can reduce microbial contamination and produce attractive flavors due to Maillard reaction. However, thermal processing of fish and meat can produce undesirable mutagenic and/or carcinogenic agents, such as heterocyclic aromatic amines (HAAs) and advanced glycation end products (AGEs) (Cao et al., 2020, Cross and Sinha, 2004, Quan et al., 2020).
Both the two harmful substances are usually produced by thermal processing (Hamzalıoğlu & Gökmen, 2020). HAAs are mostly derived from pyrolysis reactions of proteins or amino acids during thermal processing of fish and meat, especially by roasting, frying, grilling (Adeyeye & Ashaolu, 2021). To date, over 30 HAAs have been isolated and identified at ng/g levels in cooked foods and the common HAAs can be found in cooked foods are 2-amino-3-methyl-imidazo [4,5-f]quinoline (IQ), 2-amino-3-methylimidazo [4,5-f]quinoxaline (IQx), 2-amino3,4-dimethylimidazo [4,5-f]quinoline (MeIQ), 2-amino-3,8dimethylimidazo [4,5-f] quinoxaline (MeIQx), 2-amino-1methyl-6-phenylimidazo [4,5-b]pyridine (PhIP), 3-Amino-1,4-dimethyl-5H-pyrido[4,3-b]indole (Trp-P-1), 3-Amino-1-methyl-5H-pyrido[4,3-b]indole (Trp-P-2), 2-Amino-9H-dipyrido[2,3-b]indole (AαC), 2-Amino-3-methyl-9H-dipyrido[2,3-b]indole (MeAαC), 9H-pyrido[3,4-b]indole (Norharman) and 1-methyl-9H-pyrido[3,4-b]indole (Harman) (Barzegar et al., 2019, Gibis & Monika, 2016, Khan et al., 2019, Rahman et al., 2014). The formation of HAAs is closely related to the Maillard reaction, the participation of the Maillard reaction can be utilized both to inhibit and enhance HAAs formation, that was proposed and verified by the isotope labeling method, moreover, the HAAs precursors are found to be the Maillard reaction products, creatine, creatinine, amino acids or dipeptides and reducing sugars, etc (Skog, Johansson, & Jägerstad, 1995). AGEs in food are formed by nonenzymatic glycosylation of reducing sugars and protein amino groups, which are a series of harmful products produced at the final stages of the Maillard reaction (Goldin, Beckman, Schmidt, & Creager, 2006). A range of dietary AGEs have been isolated and identified in various thermal-processed foods, like meat and fish products, and potato-based foods (Yu et al., 2018, Yu et al., 2021), while the most typical dietary AGEs are Nε-(carboxymethyl)lysine (CML) and Nε-(carboxyethyl)lysine (CEL). The two common AGEs CML and CEL are presented in many thermal processed food, which are generated from the reaction of lysine and glyoxal produced by oxidation /degradation of sugar or the oxidation of Amadori product during thermal processing and lipid peroxidation (Nguyen et al., 2016, Zhu et al., 2021). Interestingly, both HAAs and AGEs increase with increasing temperature and heating time, and they contain similar formation pathways (Malliard reaction), precursors (glucose, amino acids) and some intermediates (ketones and aldehydes with active carbonyl group, Amadori rearrangement products), active carbonyl compounds and free radicals contributes their production (Zhang, Wang, & Fu, 2020).
Given the threat associated with HAAs and AGEs to human health, it is necessary to reduce their formation. Both the two harmful substances are generated synchronously, however, their inhibition methods are always studied separately. Antioxidant agents have been given special attention to inhibit HAAs and AGEs in model and real food system. Various phenolic compounds, such as ginger and curcumin (Xue et al., 2022), catechin (Kokkinidou & Peterson, 2014), (–)-epicatechin (Totlani & Peterson, 2006), (–)-epigallocatechin-3-gallate (EGCG) (Bin, Peterson, & Elias, 2012) and some hydrocolloids (Zhang et al., 2021), due to their ability of radical and dicarbonyl intermediates scavenging, amine group blocking (Guerra & Yaylayan, 2014), have been reported to inhibit the formation of HAAs and AGEs in cooked meat (Salazar, Arámbula-Villa, Hidalgo, & Zamora, 2014). Vegetables extracts that are rich in polyphenols as a safe and easy acquiring natural antioxidant, may be useful additives in thermal processing foods for inhibiting toxic HAAs and AGEs (Gibis, 2007), meanwhile, they are essential in our daily diet, dietary fiber, vitamins, polyphenols, flavonoids and trace elements in vegetables extracts, are beneficial to human body. Beetroot (Beta vulgaris) and beetroot juice exhibited good results in the alleviation of the Maillard reaction products and inhibition of HAAs formation (Račkauskienė et al., 2015). Sonchus olearleu (a kind of Chinese edible wild plant) extract and artichoke extract can effectively inhibit HAAs generation (Tengilimoglu-Metin et al., 2017, Teng et al., 2019). However, the few findings are focused on pork or beef, not on fish, and the application of common vegetables. Therefore, it will be a prospective area to exploit vegetables extracts and applied them to HAA and AGEs inhibition; moreover, the explanation of vegetables extracts' chemical intervention on HAA, AGEs formation is a crucial issue.
This study aims to investigate the formation of harmful HAAs, CML and CEL in roasted mackerel, evaluate the inhibitory effects of vegetables extracts (including celery, carrot and yam extracts) on these harmful substances and explore the possible inhibitory mechanism involved. We hope that this work could open a new function of vegetables extracts and their potential applications in food safety processing, more importantly, provide practical applications for harmful substances control in roasted mackerel and may be applicable to various meat systems.
Section snippets
Raw materials
Fresh mackerel was purchased from local Changxing market (Dalian, China). Fresh mackerel were killed using stunning by trained personnel, and placed with ice bags back to laboratory in 40 min. We then minced with a kitchen blender to obtain mackerel surimi in laboratory. The soybean oil was bought from the supermarket. The food grade extracts of celery, carrot and yam were both obtained from Yixin biology Co., Ltd (Henan, China), which were extracted from raw materials through a series of
Quantification of HAAs, CML and CEL in roasted mackerel at different temperatures
HAAs have been identified in thermal processed meat products and their formation is principally depend on temperature (Murkovic, 2004). The chromatograms and standard curve of 13 HAAs standards, including IQ, IQX, MeIQ, 8-MeIQX, 4,8-DiMeIQX, 7,8-DiMeIQX, Trp-p-1, Trp-p-2, PhIP, AαC, MeAαC, Harman and Norharman, were firstly measured and presented in Fig. S1. The limits of detection (LOD, 0.1–0.3 ng/g) and quantification (LOQ, 0.5–1.0 ng/g) of 13 individual HAAs are showed to evaluate HAAs
Conclusion
In conclusion, the present research demonstrates a novel route to use vegetable extracts as a new kind of HAAs and AGEs formation inhibitor in roasted mackerel. In addition to playing a role of affecting the total amount of HAAs, CML and CEL, the introduction of vegetable extracts not only helps in protecting the quality of the mackerel against the lipid and protein oxidation and the nutrition loss of high quality polyunsaturated fatty acids (EPA + DHA), but also enhances the flavor to a
CRediT authorship contribution statement
Simin Zhang: Methodology, Software, Writing – original draft. Ruichun Wang: Validation, Supervision. Junbo Chu: Formal analysis, Data curation. Chenyang Sun: Investigation, Software. Songyi Lin: 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 work was financially supported by the National Natural Science Foundation of China (31901723) and the Basic Scientific Research project of Liaoning Province (LJKZ0548).
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