Antioxidant activity of Maillard reaction products derived from stingray (Himantura signifier) non-protein nitrogenous fraction and sugar model systems

https://doi.org/10.1016/j.lwt.2014.01.042Get rights and content

Highlights

  • Antioxidant activity of the MRPs from stingray NPN–sugar was evaluated.

  • Antioxidant activity of stingray NPN can be improved by Maillard reaction.

  • Stingray NPN–sugar MPRs can be applied as a potential antioxidant in food products.

Abstract

This study aimed to evaluate the antioxidant activity of the Maillard reaction products (MRPs) derived from stingray non-protein nitrogenous (NPN) fraction and sugar (glucose, galactose and fructose) model systems. MRPs were prepared by heating the solution containing NPN (2 g nitrogen/100 ml) and sugar (2 g/100 ml) in 0.05 M sodium hydrogen carbonate buffer, pH 12 for 120 min at 100 °C. Reducing power and capacity to scavenge hydrogen peroxide (H2O2), hydroxyl radical (OHradical dot), 2,2′-azinobis(3-ethylbenzothiazoline-6-sulfonate) radical (ABTSradical dot+) and 2,2-diphenyl-1-picrylhydrazyl radical (DPPHradical dot) of all MRPs were greater than those of original NPN solution (P < 0.05). The MRPs derived from NPN–fructose tended to have the highest reducing capacity and free radical scavenging ability. However, the ferrous (Fe2+) chelating activity of all MRPs was lower than the original NPN solution (P < 0.05). Therefore, reducing power and scavenging activity toward free radicals and reactive oxygen species of NPN from stingray muscle can be improved significantly by reacting NPN with sugar particularly fructose via the Maillard reaction. However, the Maillard reaction seemed to show a negative impact on the Fe2+ chelating activity of stingray NPN.

Introduction

Nitrogenous compounds are very important components of fish meat and affect both nutritional value and sensory properties of fish products. The major nitrogenous compounds of fish flesh are protein and NPN compounds. The contents of NPN compounds in fish depend on the species, the habitat, life cycle and state of freshness after catch (Sikorski, 1994). NPN makes up generally 9–15 g/100 g of the total nitrogen in the meat of marine white fish, 16–18 g/100 g in clupeides and up to 55 g/100 g in sharks (Finne, 1992, Shahidi, 1995, Sikorski, 1994). About 95% of the total amount of NPN in the muscle of marine fish is composed of free amino acids, imidazole dipeptides, trimethylamineoxide (TMAO) and its degradation products, urea, guanidine compounds, nucleotides and the products of their postmortem changes and betaines (Ikeda, 1979, Sikorski, 1994). The main peptides found in fish meat are carnosine, anserine and balenine (ophidine) (Sikorski, 1994). Numerous studies indicated that low-molecular weight water-soluble NPN compounds such as polyamines (e.g. spermine and spermidine), histidine-containing dipeptides (particularly carnosine, anserine, balenine), nucleotides, and glutathione tripeptide have excellent potential for use as natural food antioxidants (Kanner et al., 1987, LØvaas, 1991, Reische et al., 1997, Sasaki et al., 1996). Liwa, Chaijan, and Manurakchinakorn (2011) examined the NPN content in whole muscle of 4 fish species including Indian mackerel (Rastrelligar kanagurta), threadfin bream (Nemipterus bleekeri), stingray (Himantura signifier) and tilapia (Oreochromis niloticus) at the same postmortem period. These fish were selected for representing marine teleost dark-fleshed fish, marine teleost white-fleshed fish, marine cartilaginous (elasmobranch) fish and fresh water teleost fish, respectively. It was found that stingray muscle contained the highest amount of NPN. At the equal nitrogen content, stingray NPN exhibited the highest OHradical dot and H2O2 scavenging activities and metal chelating ability compared with the others (Liwa et al., 2011).

The Maillard reaction is generally regarded as an efficient and safe method to improve functional properties of proteins such as solubility, heat stability, emulsifying properties, anti-allergenicity and antioxidant activity (Guo & Xiong, 2013). It has been reported that MRPs pronounced antioxidative effects in vitro, in vivo and in food systems (Chuyen, Ijichi, Umetsu, & Moteki, 1998). MRPs, especially melanoidins, have antioxidant activity through scavenging oxygen radicals or chelating metals. However, compounds in the MRPs with amino reductone structures may have both antioxidant and pro-oxidant activities depending on the reaction conditions (Pischetsrieder, Rinaldi, Gross, & Severin, 1998). MRPs have been used to prevent lipid oxidation in many products. Lipid foods have been relatively stable when the Maillard reaction was involved (Chuyen et al., 1998). The antioxidative property of MRPs was found in potato chips (Kato, Chuyen, Utsunomiya, & Okitani, 1986), biscuit and cookies (Yamaguchi, Koyama, & Fujimaki, 1981), sausages (Lingnert & Ericksson, 1981), ground pork patties (Bedinghaus & Ockerman, 1995), cooked ground beef (Alfawaz et al., 1994, Bailey, 1988) and cooked beef patties (Fernandez, Sturla, Doval, Romero, & Judis, 2012). Furthermore, MRPs can prevent the oxidation of sardine lipid (Chiu, Tanaka, Nagashima, & Tagushi, 1991) and can be used as soaking agent to retard the oxidation of lipid and myoglobin in mackerel fillet prior to keep refrigeration (Chaijan, Kewmanee, Hirunkan, Aryamuang, & Panpipat, 2009).

Any nitrogenous compound can be used as a substrate for the Maillard reaction. Thus, NPN fraction can be used as an alternative substrate for the Maillard reaction. However, NPN fraction originally showed the antioxidant activity. Positive or negative impact of the Maillard reaction on antioxidant capacity of NPN has not been reported. In addition, no information regarding the antioxidant activity of MRPs derived of fish NPN, particularly from stingray muscle, and sugar has been reported. Therefore, the objective of this study was to evaluate the antioxidant activity of MRPs produced from stingray NPN and sugar (glucose, fructose and galactose) model system. Analyses of free radical and reactive oxygen species scavenging activities, reducing power and metal chelation of produced MRPs were done in comparison with those of original NPN solution.

Section snippets

Chemicals

DPPH, ABTS, deoxyribose, potassium ferricyanide (K3Fe(CN6)) and 3-(2-pyridyl)-5,6-bis(4-phenyl-sulfonic acid)-1,2,4-triazine (ferrozine) were purchased from Sigma–Aldrich (St. Louis, MO, USA). Trichloroacetic acid (TCA) was obtained from Riedel-deHaen (Seelze, Germany). Glucose, galactose, fructose, ferric chloride, H2O2 and thiobarbituric acid (TBA) were obtained from Fluka (Buchs, Switzerland).

Fish samples

Stingrays with an average weight of 0.5–1 kg were caught from Thasala–Nakhon Si Thammarat Coast

Reducing power

It has been reported that compounds responsible for reducing activity are formed during thermolysis of Amadori products in the primary phase of the Maillard reactions (Hwang, Shue, & Chang, 2001) or could be heterocyclic products of the Maillard reaction or caramelization of sugars (Charurin, Ames, & Castiello, 2002). Moreover, MRPs could function as electron donors and hydroxyl (OH) and pyrrole groups of advanced MRPs may act as reducing agents (Yanagimoto et al., 2002, Yoshimura et al., 1997

Conclusions

Heat treatment of stingray NPN–sugar model system produced MRPs which possessed antioxidative activity. Reducing power and scavenging activity toward free radicals and reactive oxygen species of NPN from stingray muscle can be improved significantly by reacting NPN with sugar especially fructose via the Maillard reaction. However, the Maillard reaction seemed to have a detrimental effect on the chelating activity of stingray NPN. MRPs derived from stingray NPN–sugar can function as both primary

Acknowledgment

This work was supported by Walailak University Fund and the TRF Senior Scholar Program.

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