7
Review Marine food-derived functional ingredients as potential antioxidants in the food industry: An overview Dai-Hung Ngo a , Isuru Wijesekara a , Thanh-Sang Vo a , Quang Van Ta a , Se-Kwon Kim a,b, a Marine Biochemistry Laboratory, Department of Chemistry, Pukyong National, University, Busan 608-737, Republic of Korea b Marine Bioprocess Research Center, Pukyong National University, Busan 608-737, Republic of Korea abstract article info Article history: Received 21 October 2010 Accepted 15 December 2010 Keywords: Antioxidants Bioactive peptides Chitooligosaccharides Sulfated polysaccharides Phlorotannins Recently, a great deal of interest has been developed by the consumers towards natural bioactive compounds as functional ingredients in the food products due to their various health benecial effects. Hence, it can be suggested that antioxidative functional ingredients from marine foods and their by-products are alternative sources for synthetic ingredients that can contribute to a consumer's well-being, as a part of nutraceuticals and functional foods. This contribution presents an overview of the marine food-derived antioxidants such as bioactive peptides, chitooligosaccharide derivatives, sulfated polysaccharides, phlorotannins and carotenoids with the potential utilization in the food industry. © 2010 Elsevier Ltd. All rights reserved. Contents 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 523 2. Development of marine food-derived antioxidative ingredients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 524 3. Marine food-derived antioxidants and their antioxidative activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 524 3.1. Bioactive peptides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 524 3.2. Chitooligosaccharide derivatives (COS) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 525 3.3. Sulfated polysaccharides (SPs) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 525 3.4. Phlorotannins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 526 3.5. Carotenoids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 526 4. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 527 Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 527 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 527 1. Introduction Antioxidants may have a positive effect on human health as they can protect the human body against damage by reactive oxygen species (ROS), which attack macromolecules such as membrane lipids, proteins and DNA, lead to many health disorders such as cancer, diabetes mellitus, neurodegenerative and inammatory diseases with severe tissue injuries (Buttereld et al., 2002; Frlich & Riederer, 1995; Halliwell & Aruoma, 1991; Yang, Landau, Huang, & Newmark, 2001). Moreover, the deterioration of some foods has been identied due to the oxidation of lipids or rancidity and the formation of undesirable secondary lipid peroxidation products. Lipid oxidation by ROS such as superoxide anion, hydroxyl radicals and H 2 O 2 also causes a decrease in nutritional value of lipid foods, and affect their safety and appearance. Therefore, in food and pharmaceutical industries, many synthetic commercial antioxidants such as butylated hydroxytoluene (BHT), butylated hydroxyanisole (BHA), tert-butylhydroquinone (TBHQ) and propyl gallate (PG) have been used to retard the oxidation and peroxidation processes. However, the use of these synthetic antioxidants must be under strict regulation due to potential health hazards (Hettiarachchy, Glenn, Gnanasambandan, & Johnson, 1996; Park, Jung, Nam, Shahidi, & Kim, 2001). Hence, the search for natural antioxidants as safe alternatives is important in the food industry (Penta-Ramos & Xiong, 2001). Food Research International 44 (2011) 523529 Corresponding author. Marine Biochemistry Laboratory, Department of Chemistry, Pukyong National, University, Busan 608-737, Republic of Korea. Tel.: + 82 516297097; fax: + 82 516297099. E-mail address: [email protected] (S.-K. Kim). 0963-9969/$ see front matter © 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.foodres.2010.12.030 Contents lists available at ScienceDirect Food Research International journal homepage: www.elsevier.com/locate/foodres

Marine food-derived functional ingredients as potential antioxidants in the food industry: An overview

Embed Size (px)

Citation preview

Food Research International 44 (2011) 523–529

Contents lists available at ScienceDirect

Food Research International

j ourna l homepage: www.e lsev ie r.com/ locate / foodres

Review

Marine food-derived functional ingredients as potential antioxidants in the foodindustry: An overview

Dai-Hung Ngo a, Isuru Wijesekara a, Thanh-Sang Vo a, Quang Van Ta a, Se-Kwon Kim a,b,⁎a Marine Biochemistry Laboratory, Department of Chemistry, Pukyong National, University, Busan 608-737, Republic of Koreab Marine Bioprocess Research Center, Pukyong National University, Busan 608-737, Republic of Korea

⁎ Corresponding author. Marine Biochemistry LaboratPukyong National, University, Busan 608-737, Republic ofax: +82 516297099.

E-mail address: [email protected] (S.-K. Kim).

0963-9969/$ – see front matter © 2010 Elsevier Ltd. Aldoi:10.1016/j.foodres.2010.12.030

a b s t r a c t

a r t i c l e i n f o

Article history:Received 21 October 2010Accepted 15 December 2010

Keywords:AntioxidantsBioactive peptidesChitooligosaccharidesSulfated polysaccharidesPhlorotannins

Recently, a great deal of interest has been developed by the consumers towards natural bioactive compoundsas functional ingredients in the food products due to their various health beneficial effects. Hence, it can besuggested that antioxidative functional ingredients from marine foods and their by-products are alternativesources for synthetic ingredients that can contribute to a consumer's well-being, as a part of nutraceuticalsand functional foods. This contribution presents an overview of the marine food-derived antioxidants such asbioactive peptides, chitooligosaccharide derivatives, sulfated polysaccharides, phlorotannins and carotenoidswith the potential utilization in the food industry.

ory, Department of Chemistry,f Korea. Tel.: +82 516297097;

l rights reserved.

© 2010 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5232. Development of marine food-derived antioxidative ingredients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5243. Marine food-derived antioxidants and their antioxidative activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 524

3.1. Bioactive peptides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5243.2. Chitooligosaccharide derivatives (COS) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5253.3. Sulfated polysaccharides (SPs) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5253.4. Phlorotannins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5263.5. Carotenoids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 526

4. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 527Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 527References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 527

1. Introduction

Antioxidants may have a positive effect on human health as they canprotect the human body against damage by reactive oxygen species(ROS), which attack macromolecules such as membrane lipids, proteinsandDNA, lead tomanyhealth disorders such as cancer, diabetesmellitus,neurodegenerative and inflammatorydiseaseswith severe tissue injuries(Butterfield et al., 2002; Frlich & Riederer, 1995; Halliwell & Aruoma,1991; Yang, Landau, Huang, & Newmark, 2001). Moreover, the

deterioration of some foods has been identified due to the oxidation oflipids or rancidity and the formation of undesirable secondary lipidperoxidation products. Lipid oxidation by ROS such as superoxide anion,hydroxyl radicals and H2O2 also causes a decrease in nutritional value oflipid foods, and affect their safety and appearance. Therefore, in food andpharmaceutical industries,many synthetic commercial antioxidants suchas butylated hydroxytoluene (BHT), butylated hydroxyanisole (BHA),tert-butylhydroquinone (TBHQ) and propyl gallate (PG) have been usedto retard the oxidation and peroxidation processes. However, the use ofthese synthetic antioxidants must be under strict regulation due topotential health hazards (Hettiarachchy, Glenn, Gnanasambandan, &Johnson, 1996; Park, Jung, Nam, Shahidi, & Kim, 2001). Hence, the searchfor natural antioxidants as safe alternatives is important in the foodindustry (Penta-Ramos & Xiong, 2001).

524 D.-H. Ngo et al. / Food Research International 44 (2011) 523–529

Recently, there is a considerable interest in the food industry as wellas pharmaceutical industry for the development of antioxidants fromnatural sources, such as marine flora and fauna. Marine organisms arerich sources of structurally diverse bioactive compounds with valuablenutraceutical, pharmaceutical and cosmeceutical potentials (Barrow &Shahidi, 2008; Shahidi & Zhong, 2008). Among them, marine algaerepresent one of the richest sources of natural antioxidants (Mayer &Hamann, 2002; Ruperez, 2001). It is believed that marine algae areprotected against oxidative deteriorationby certain antioxidant systems.In addition,marine food processing by-products can be easily utilized toproducing nutraceuticals and functional food ingredients with antiox-idative property (Kim &Mendis, 2006). Most of the research onmarine-derived antioxidants has focused on potency of crude extracts witheffective antioxidant compounds remainingunisolated andunidentified.Only few studies have been carried out aiming at purification andcharacterization of antioxidants from marine sources (Shahidi, 2007).This review focuses on the potential application of marine food-derivednovel antioxidants such as bioactive peptides, chitooligosaccharidederivatives, sulfated polysaccharides, phlorotannins and carotenoids inthe food industry.

2. Development of marine food-derived antioxidative ingredients

There is a great potential in marine bioprocess industry to convertand utilizemost ofmarine food products andmarine food by-productsas valuable functional ingredients. Apparently, there has been anincreasing interest in utilization of marine products and novel bio-processing technologies are developing for isolation of some bioactivesubstances with antioxidative property from marine food products tobe used as functional foods and nutraceuticals. Development of thesefunctional ingredients involves certain bio-transformation processesthrough enzyme-mediated hydrolysis in batch reactors. Membranebioreactor technology equipped with ultrafiltration membranes isrecently emerging for the bio-processing and development offunctional ingredients and considered as a potential method to utilizemarine food products efficiently (Kim & Mendis, 2006; Kim &Rajapakse, 2005; Nagai & Suzuki, 2000).

This system has the main advantage that the molecular weightdistribution of the desired functional ingredient can be controlled bythe adoption of an appropriate ultrafiltration membrane (Cheryan &Mehaia, 1990; Jeon, Byun, & Kim, 1999; Kim, Byun, Kang, & Song,1993). Enzymatic hydrolysis of marine food products allows prepa-ration of functional ingredients such as bioactive peptides andchitooligosaccharides. The physico-chemical conditions of the reac-tion media, such as temperature and pH of the reactant solution, mustthen be adjusted in order to optimize the activity of the enzyme used.Proteolytic enzymes from microbes, plants and animals can be usedfor the hydrolysis process of marine food products to developbioactive peptides and chitooligosaccharide derivatives. Moreover,one of the most important factors in producing bioactive functionalingredients with desired functional properties is themolecular weightof the bioactive compound. Therefore, for the efficient recovery and toobtain bioactive functional ingredients with both a desired molecularsize and functional property, a suitable method is the use of an

Table 1Antioxidative peptides from marine organisms.

Amino acid sequence of the peptide Source

Leu-Lys-Gln-Glu-Leu-Glu-Asp-Leu-Leu-Glu-Lys-Gln-Glu OysterPhe-Asp-Ser-Gly-Pro-Ala-Gly-Val-Leu Jumbo squidVal-Glu-Cys-Tyr-Gly-Pro-Asn-Arg-Pro-Glu-Phe MicroalgaPhe-Gly-His-Pro-Tyr Blue musselLeu-Leu-Gly-Pro-Gly-Leu-Thr-Asn-His-Ala RotiferVal-Lys-Ala-Gly-Phe-Ala-Trp-Thr-Ala-Asn-Glu-Glu-Leu-Ser TunaLeu-Gly-Leu-Asn-Gly-Asp-Asp-Val-Asn Conger eelArg-Pro-Asp-Phe-Pro-Leu-Glu-Pro-Pro-Tyr Yellowfin sole

ultrafiltrationmembrane system. In order to obtain functionally activepeptides, it is a suitable method to use a three enzymes system forsequential enzymatic digestion. Moreover, it is possible to obtainserial enzymatic digestions in a system using a multi-step recyclingmembrane reactor combined with an ultrafiltration membranesystem to bio-processing and development of marine food derivedbioactive peptides and chitooligosaccharide derivatives (Byun & Kim,2001; Jeon et al., 1999). This membrane bioreactor technologyequipped with ultrafiltration membranes is recently emerging forthe development of functional ingredients and considered as apotential method to utilize marine food products as value addednutraceuticals with beneficial health effects.

3. Marine food-derived antioxidants and their antioxidativeactivity

3.1. Bioactive peptides

Components of proteins in marine foods are containing sequencesof bioactive peptides, which could exert a physiological effect in thebody. Moreover, some of these bioactive peptides have identified topossess nutraceutical potentials that are beneficial in human healthpromotion (Defelice, 1995) and recently the possible roles of food-derived bioactive peptides in reducing the risk of cardiovasculardiseases has been reported (Erdmann, Cheung, & Schroder, 2008).Bioactive peptides usually contain 3–20 amino acid residues, and theiractivities are based on their amino acid composition and sequence(Pihlanto-Leppala, 2001). These short chains of amino acids areinactive within the sequence of the parent protein, but can be releasedduring gastrointestinal digestion, food processing, or fermentation.

Marine-derived bioactive peptides have been obtained widely byenzymatic hydrolysis of marine proteins (Kim & Wijesekara, 2010)and have shown to possess many physiological functions, includingantioxidant (Kim, Je, & Kim, 2007), antihypertensive or ACE inhibition(Yokoyama, Chiba, & Yoshikawa, 1992), anticoagulant (Rajapakse,Jung, Mendis, Moon, & Kim, 2005), and antimicrobial (Liu et al., 2008)activities. In fermented marine food sauces such as, blue mussel sauceand oyster sauce, enzymatic hydrolysis has already been done bymicroorganisms, and bioactive peptides can be purified withoutfurther hydrolysis. In addition, marine processing by-products containbioactive peptides with valuable functional properties (Kim &Mendis,2006). Recently, a number of studies have shown that peptidesderived from various marine protein hydrolysates can be used aspotential antioxidants (Table 1). The antioxidant activity of marine-derived bioactive peptides has been determined by various in vitromethods, such as DPPH, peroxide, hydroxyl and superoxide anionradical scavenging activities which have been detected by electronspin resonance (ESR) spectroscopy method as well as intra cellularfree radical scavenging assays, such as DNA oxidation, reactive oxygenspecies scavenging, membrane protein oxidation and membrane lipidoxidation. The hydrophobic amino acids present in the peptidesequence contribute greatly for their potential antioxidant activity(Mendis, Rajapakse, Byun, & Kim, 2005; Mendis, Rajapakse, & Kim,2005). Furthermore, several studies have been indicated that peptides

Ref.

Qian et al., 2008Mendis, Rajapakse, Byun, et al., 2005; Mendis, Rajapakse, & Kim, 2005Sheih, Wu, & Fang, 2009Jung, Rajapakse, & Kim, 2005Byun, Lee, Park, Jeon, & Kim, 2009Je, Qian, Byun, & Kim, 2007Ranathunga, Rajapakse, & Kim, 2006Jun et al., 2004

525D.-H. Ngo et al. / Food Research International 44 (2011) 523–529

derived frommarinefishproteins have greater antioxidant properties indifferent oxidative systems (Jun, Park, Jung, & Kim, 2004). However, theexact mechanism of peptides to act as antioxidants are not clearlyknownbut somearomatic aminoacids andhistidine are reported toplaya vital role for the activity. Most of marine food-derived bioactivepeptides have shown higher antioxidative potential thanα-tocopherol.For example, the peptide (Glu-Ser-Thr-Val-Pro-Glu-Arg-Thr-His-Pro-Ala-Cys-Pro-Asp-Phe-Asn) which isolated from the peptic hydrolysateof hoki (Johnius belengerii) frame protein has inhibited lipid peroxida-tion higher than that of α-tocopherol as positive control and efficientlyquencheddifferent sources of free radicals (Kimet al., 2007). Inaddition,the peptide (Leu-Lys-Gln-Glu-Leu-Glu-Asp-Leu-Leu-Glu-Lys-Gln-Glu)obtained by the gastro-intestinal digestion of oyster (Crassostrea gigas)has exhibited a greater activity against polyunsaturated fatty acidsperoxidation than α-tocopherol (Qian, Jung, Byun, & Kim, 2008).

Therefore, marine derived bioactive peptides with antioxidativeproperties may have great potential for use as functional ingredients infunctional foods and nutraceuticals instead of synthetic antioxidants.For example, Shahidi,Han, and Synowiecki (1995) clearly demonstratedthat Capelin fish protein hydrolysate which added to minced porkmuscle at a level of 0.5–3.0% reduced the formation of secondaryoxidation products including thiobarbituric acid reactive substances theproduct by17.7–60.4%. However, the bitter taste of protein hydrolysatesprevents the use of bioactive peptides as food additives (Kristinsson &Rasco, 2000) and the bioactivity may be reduced through molecularalteration during food processing or interaction with other foodingredients (Moller, Scholz-Ahrens, Roos, & Schrezenmeir, 2008). As atreatment to this bitterness, Shahidi et al. (1995) treated fish proteinhydrolysate with activated carbon, which removed bitter peptides. Thechallenge for food technologists will be to develop functional foods andnutraceuticals without the undesired side effects of the added peptides.

3.2. Chitooligosaccharide derivatives (COS)

Chitin is the second most abundant biopolymer on earth aftercellulose and one of the most abundant polysaccharides. It is a glycanof β (1→4)-linked N-acetylglucosamine units and it is widelydistributed in crustaceans and insects as the protective exo-skeletonand cell walls of most fungi. Chitin is usually prepared from the shellsof crabs and shrimps. Chitosan (Fig. 1), a partially deacetylatedpolymer of N-acetylglucosamine, is prepared by alkaline deacetyla-tion of chitin (Kim, Nghiep, & Rajapakse, 2006). COS are chitosanderivatives (polycationic polymers comprised principally of glucos-amine units) and can be generated via either chemical or enzymatichydrolysis of chitosan (Jeon & Kim, 2000a;2000b). Recently, COS havebeen the subject of increased attention in terms of their pharmaceu-tical and medicinal applications (Kim & Rajapakse, 2005), due to theirmissing toxicity and high solubility as well as their positivephysiological effects such as antioxidant (Park, Je, & Kim, 2003), ACEenzyme inhibition (Hong, Kim, Oh, Han, & Kim, 1998), antimicrobial(Park et al., 2003), anticancer (Jeon & Kim, 2002), antidiabetic (Liu,Liu, Han, & Sun, 2007), hypocholesterolemic (Kim et al., 2005),hypoglycemic (Miura, Usami, Tsuura, Ishida, & Seino, 1995), anti-Alzheimer's (Yoon, Ngo, & Kim, 2009), anticoagulant (Park, Lee, &Kim, 2004) properties and adipogenesis inhibition (Cho et al., 2008).

Radical scavenging activity of COS depends on their degree ofdeacetylation values andmolecular weights. According to the electron

Fig. 1. Structure of chitosan.

spin resonance studies, 90% deacetylated medium molecular weighthetero-COS have the highest free radical scavenging activity of all freeradicals tested such as DPPH, hydroxyl, superoxide and carboncentered radicals (Je, Park, & Kim, 2004). Inhibition of free-radicalmediated oxidation of cellular biomolecules such as lipids, proteinsand direct scavenging of reactive oxygen species by carboxylatedchitooligosaccharides (CCOS) has been reported (Rajapakse, Kim,Mendis, & Kim, 2007). Moreover, the cellular antioxidant effects ofchitin oligosaccharides (NA-COS) produced by acidic hydrolysis ofcrab shell chitin were reported by Ngo, Lee, Kim, and Kim (2009).NA-COS can inhibit myeloperoxidase activity and decrease free-radical oxidation of DNA and membrane proteins. Moreover, chitosanat an addition of 0.02% had antioxidant effects in lard and cruderapeseed oil but the activity was less than ascorbic acid (Xia, Liu,Zhang, & Chen, 2010). In the food industry, chitosan (edible chitosan,more than 83% degree of deacetylation) and COS have been used asDietary Food Additives and functional factors for their healthbeneficial effects as well as drug carriers (Xia et al., 2010). Therefore,the application of COS as antioxidants in the food industry is promising.

3.3. Sulfated polysaccharides (SPs)

In recent years, various sulfated polysaccharides (SPs) isolatedfrommarine algae have attracted much attention in the fields of food,pharmaceutical and cosmetic industries. SPs comprise a complexgroup of macro-molecules with a wide range of important biologicalactivities. These polymers are chemically anionic and widespread notonly in marine algae but also occur in animals such as mammals andinvertebrates (Mourao, 2007; Mourao & Pereira, 1999). Marine algaeare the most important source of non-animal SPs and their chemicalstructures (Fig. 2) vary according to the species of algae such asfucoidan in brown algae (Phaeophyceae), carrageenan in red algae(Rhodophyceae), and ulvan in green algae (Chlorophyceae) (Costa etal., 2010). These SPs exhibited various health beneficial biologicalactivities such as anti-HIV-1 (Schaeffer & Krylov, 2000), anticoagulant(Chevolot et al., 1999; McLellan & Jurd, 1992), immunomodulating(Leiro, Castro, Arranz, & Lamas, 2007) and anticancer (Rocha et al.,2005) activities.

In the last decade, it has been reported that some marine algaederived SPs can be used as potential antioxidants (Kim, Choi, et al.,2007; Qi et al., 2005; Rocha de Souza et al., 2007; Ruperez, Ahrazem, &Leal, 2002; Wang, Zhang, Zhang, & Li, 2008; Zhang et al., 2003). Theantioxidant activity of SPs have been determined by various methodssuch as 1,1-diphenyl-2-picryl hydrazil (DPPH) radical scavenging,lipid peroxide inhibition, ferric reducing antioxidant power (FRAP),nitric oxide (NO) scavenging, ABTS radical scavenging, superoxideradical and hydroxyl radical scavenging assays. In addition, Xue, Yu,Hirata, Terao, and Lin (1998) reported that several marine-derivedSPs have antioxidative activities in phosphatidylcholine-liposomalsuspension and organic solvents. According to Kim, Choi, et al. (2007)the SPs of Sargassum fulvellum (Phaeophyceae), is more potentNO scavenger than commercial antioxidants such as BHA andα–tocophorol. Antioxidant activity of SPs depends on their structuralfeatures such as degree of sulfating, molecular weight, type of themajor sugar and glycosidic branching (Qi et al., 2005; Zhang et al.,2003). For example, low molecular weight SPs have shown potentantioxidant activity than high molecular weight SPs (Sun, Wang, Shi,& Ma, 2009). The rationale for this is low molecular weight SPs mayincorporate into the cells more efficiently and donate protoneffectively compared to high molecular weight SPs. Furthermore,SPs from marine algae are known to be important free-radicalscavengers and antioxidants for the prevention of oxidative damage,which is an important contributor in carcinogenesis. Collectively,these evidences suggest that marine food-derived SPs prove to be oneof the useful candidates in the search of effective, non-toxicsubstances with potential antioxidant activity. Moreover, SPs are

Fig. 2. Monomeric units of antioxidative sulfated polysaccharides from marine algae (a) fucoidan, (b) carrageenan, and (c) ulvan.

526 D.-H. Ngo et al. / Food Research International 44 (2011) 523–529

by-products in the preparation of alginates from edible brownseaweeds and could be used as a rich source of natural antioxidantswith potential application in the food industry.

3.4. Phlorotannins

Phlorotannins are phenolic compounds formed by the polymer-ization of phloroglucinol or defined as 1,3,5-trihydroxybenzenemonomer units and biosynthesized through the acetate–malonatepathway. They are highly hydrophilic components with a wide rangeof molecular sizes ranging between 126 and 650,000 Da (Ragan &Glombitza, 1986). Marine brown algae accumulate a variety ofphloroglucinol-based polyphenols, as phlorotannins could be usedas functional ingredients in nutraceuticals with potential health effects(Wijesekara, Yoon, &Kim, 2010). Amongmarine algae, Ecklonia cava; anedible brown algae is a rich source of phlorotannins than others (Heo,Park, Lee, & Jeon, 2005). Phlorotannins have several health beneficialbiological activities including, antioxidant (Li et al., 2009), anti-HIV(Artan et al., 2008), antiproliferative (Kong, Kim, Yoon, & Kim, 2009),anti-inflammatory (Jung et al., 2009), radioprotective (Zhang et al.,2008), antidiabetic (Lee, Li, Karadeniz, Kim, & Kim, 2009), anti-Alzheimer's disease (acetyl- and butyryl-cholinesterase inhibitory)(Yoon, Lee, Li, & Kim, 2009), antimicrobial (Nagayama, Iwamura,Shibata, Hirayama, & Nakamura, 2002) and antihypertensive (Jung,Hyun, Kim, & Choi, 2006) activities.

Most of phlorotannins which purified from marine brown algaeare responsible for antioxidant activities and shown protective effectsagainst hydrogen peroxide-induced cell damage (Kang et al., 2005;Kang et al., 2005; Kang et al., 2006). Phlorotannins act as free radicalscavengers, reducing agents and metal chelators, and thus effectivelyinhibit lipid oxidation. According to the significant results of totalantioxidant activity compared to tocopherol as positive control in thelineloic acid model system, the phlorotannins presented a greatlyinteresting potential against 1,1-diphenyl 1,2-picrylhydrazyl (DPPH),hydroxyl, superoxide, and peroxyl radicals in vitro (Li et al., 2009). Inaddition, eckol, phlorofucofuroeckol A, dieckol, and 8,8′-bieckol haveshown a potent inhibition of phospholipid peroxidation in a liposomesystem (Shibata, Ishimaru, Kawaguchi, Yoshikawa, & Hama, 2008).These findings suggest that phlorotannins, the natural antioxidantcompounds found in edible brown algae, can protect food productsagainst oxidative degradation as well as preventing and/or treatingfree radical-related diseases.

3.5. Carotenoids

Carotenoids are a family of pigmented compounds which aresynthesized by plants, algae, fungi and microorganisms, but notanimals. They are the most important pigments in nature that areresponsible for various colors of different photosynthetic organisms(Rao & Rao, 2007). Carotenoids are thought to be responsible for thebeneficial properties in preventing human diseases including cardio-vascular diseases, cancer and other chronic diseases (Agarwal & Rao,2000). Carotenoid pigments have antioxidant properties by virtue oftheir highly unsaturated nature, which enable them to lendthemselves to oxidation instead of other molecules. The antioxidantactions of carotenoids are based on their singlet oxygen quenchingproperties and their ability to trap free radicals, which mainlydepends on the number of conjugated double bonds of the moleculeand carotenoid end groups or the nature of substituents incarotenoids containing cyclic end groups (Britton, 1995; Stahl &Sies, 1996). Fucoxanthin and astaxanthin (Fig. 3) are known to bemajor ingredients of marine carotenoids and have also beenrecognized to possess excellent antioxidative potential (Kobayashi &Sakamoto, 1999; Miyashita & Hosokawa, 2008; Simpson, 2007; Yan,Chuda, Suzuki, & Nagata, 1999).

In a recent study, Nishida, Yamashita, and Miki (2007) demon-strated that carotenoids have stronger singlet oxygen quenchingactivities thanα-tocopherol as well asα-lipoic acid and have reportedthat fucoxanthin from the brown algae Undaria pinnatifida andLaminaria japonica was one of the active compounds. Fucoxanthinderived from the brown alga U. pinnatifida and fucoxanthinolwhich prepared from fucoxanthin by hydrolysis with lipase areeffective on scavenging of 1,1-diphenyl-2-picrylhydrazyl (DPPH)and 2,2′-Azinobis-3-ethylbenzo thizoline-6-sulphonate radicals(Sachindra et al., 2007). Furthermore, the cytoprotective effect offucoxanthin, from a brown alga Sargassum siliquastrum, againstH2O2-induced cell damage has been reported by Heo et al. (2008).Fucoxanthin can effectively inhibit intracellular reactive oxygenspecies (ROS) formation, DNA damage, and apoptosis induced byH2O2. Noticeably, fucoxanthin also exhibited a strong enhance of cellviability against H2O2 induced oxidative damage. Moreover, fucoxan-thin has the potential to prevent UV-B induced cell injury in humandermal fibroblasts (HDF cells) (Heo & Jeon, 2009).

Astaxanthin is also used not only as a source of pigment in the diet,but also has potential clinical applications due to its higher an

Fig. 3. Marine-derived carotenoids, (a) astaxanthin, and (b) fucoxanthin.

527D.-H. Ngo et al. / Food Research International 44 (2011) 523–529

extremely versatile antioxidant activity than β-carotene andα-tocopherol (Miki, 1991). The higher anti-oxidant activity ofastaxanthin than other carotenoids has explained to be due to thepresence of the hydroxyl and keto endings on each ionone ring in thestructure of astaxanthin (Turujman, Wamer, Wei, & Albert, 1997). Inaddition, astaxanthin is effective against UVA-induced DNA altera-tions in human dermal fibroblasts, human melanocytes, and humanintestinal cells (Lyons & O'Brien, 2002). Moreover, consumption ofastaxanthin from marine animals leads to inhibit low-densitylipoprotein oxidation (Iwamoto et al., 2000). Furthermore, astax-anthin is effective as α-tocopherol in inhibiting free radical-initiatedlipid peroxidation in rat liver microsomes (Palozza & Krinsky, 1992),and is 100 times higher than α-tocopherol in protecting ratmitochondria against Fe2+-catalyzed lipid peroxidation in vivo andin vitro (Kurashige, Okimasu, Inoue, & Utsumi, 1990). These resultssuggest that marine-derived carotenoids such as fucoxanthin andastaxanthin are bioactive natural functional ingredients that may beimportant in human health as potential antioxidants.

4. Conclusions

Recent studies have provided evidence that marine derivedfunctional ingredients play a vital role in human health and nutrition.Moreover, the formation of cancer cells in human body can be directlyinduced by free radicals and natural anticancer drugs as chemopreven-tive agents have gained a positive popularity in treatment of cancer.Hence, radical scavenging compounds such as bioactive peptides, COS,SPs, phlorotannins, and carotenoids pigments including fucoxanthinand astaxanthin from marine foods and their by-products can be usedindirectly as functional ingredients to reduce cancer formation inhuman body. Collectively, the wide range of biological activitiesassociated with the antioxidative ingredients which derived frommarine food sources have the potential to expand its health beneficialvalue not only in the food industry but also in the pharmaceutical andcosmeceutical industries.

Acknowledgement

This study was supported by a grant from Marine BioprocessResearch Center of theMarine Bio 21 Project funded by theMinistry ofLand, Transport and Maritime, Republic of Korea.

References

Agarwal, S., & Rao, A. V. (2000). Carotenoids and chronic diseases. Drug Metabolism andDrug Interactions, 17, 189−210.

Artan, M., Li, Y., Karadeniz, F., Lee, S. H., Kim, M. M., & Kim, S. K. (2008). Anti-HIV-1activity of phloroglucinol derivative, 6, 6′-bieckol, from Ecklonia cava. Bioorganicand Medicinal Chemistry, 16, 7921−7926.

Barrow, C., & Shahidi, F. (2008). Marine nutraceuticals and functional foods. New York,USA: CRC Press.

Britton, G. (1995). Structure and properties of carotenoids in relation to function. FASEBJournal, 9, 1551−1558.

Butterfield, D. A., Castenga, A., Pocernich, C. B., Drake, J., Scapagnini, G., & Calabrese, V.(2002). Nutritional approaches to combat oxidative stress in Alzheimer's disease.Journal of Nutritional Biochemistry, 13, 444−461.

Byun, H. G., & Kim, S. K. (2001). Purification and characterization of angiotensin Iconverting enzyme (ACE) inhibitory peptides from Alaska Pollack (Theragrachalcogramma) skin. Process Biochemistry, 36, 1155−1162.

Byun, H. G., Lee, J. K., Park, H. G., Jeon, J. K., & Kim, S. K. (2009). Antioxidant peptidesisolated from the marine rotifer, Brachionus rotundiformis. Process Biochemistry, 44,842−846.

Cheryan, M., & Mehaia, M. A. (1990). Membrane bioreactors: Enzyme process. In H.Schwartzberg, & M. A. Rao (Eds.), Biotechnology and food process engineering. NewYork: Marcell Dekker.

Chevolot, L., Foucault, A., Chaubet, F., Kervarec, N., Sinquin, C., Fisher, A. M., et al. (1999).Further data on the structure of brown seaweed fucans: Relationships withanticoagulant activity. Carbohydrate Research, 319, 154−165.

Cho, E. J., Rahman, A., Kim, S. W., Baek, Y. M., Hwang, H. J., Oh, J. Y., et al. (2008). Chitosanoligosaccharides inhibit adipogenesis in 3 T3-L1 adipocytes. Journal of Microbiologyand Biotechnology, 18(1), 80−87.

Costa, L. S., Fidelis, G. P., Cordeiro, S. L., Oliveira, R. M., Sabry, D. A., Camara, R. B. G., et al.(2010). Biological activities of sulfated polysaccharides from tropical seaweeds.Biomedicine and Pharmacotherapy, 64, 21−28.

Defelice, S. L. (1995). The nutritional revolution: Its impact on food industry R & D.Trends in Food Science and Technology, 6, 59−61.

Erdmann, K., Cheung, B. W. Y., & Schroder, H. (2008). The possible roles of food-derivedbioactive peptides in reducing the risk of cardiovascular disease. Journal ofNutritional Biochemistry, 19, 643−654.

Frlich, I., & Riederer, P. (1995). Free radical mechanisms in dementia of Alzheimer typeand the potential for antioxidative treatment. Drug Research, 45, 443−449.

Halliwell, B., & Aruoma, O. I. (1991). DNA damage by oxygen derived species. Itsmechanism and measurement in mammalian systems. FEBS Letters, 281, 9−19.

Heo, S. J., & Jeon, Y. J. (2009). Protective effect of fucoxanthin isolated from Sargassumsiliquastrum on UV-B induced cell damage. Journal of Photochemistry andPhotobiology B: Biology, 95, 101−107.

Heo, S. J., Ko, S. C., Kang, S. M., Kang, H. S., Kim, J. P., Kim, S. H., et al. (2008).Cytoprotective effect of fucoxanthin isolated from brown algae Sargassumsiliquastrum against H 2O2-induced cell damage. European Food Research andTechnology, 228, 145−151.

Heo, S. J., Park, E. U., Lee, K. W., & Jeon, Y. J. (2005). Antioxidant activities of enzymaticextracts from brown seaweeds. Bioresource Technology, 96, 1613−1623.

Hettiarachchy, N. S., Glenn, K. C., Gnanasambandan, R., & Johnson, M. G. (1996). Naturalantioxidant extract from fenugreek (Trigonella foenumgraecum) for ground beefpatties. Journal of Food Science, 61, 516−519.

528 D.-H. Ngo et al. / Food Research International 44 (2011) 523–529

Hong, S. P., Kim, M. H., Oh, S. W., Han, C. H., & Kim, Y. H. (1998). ACE inhibitory andantihypertensive effect of chitosan oligosaccharides in SHR. Korean Journal of FoodScience and Technology, 30, 1476−1479.

Iwamoto, T., Hosoda, K., Hirano, R., Kurata, H., Matsumoto, A., Miki, W., et al. (2000).Inhibition of low-density lipoprotein oxidation by astaxanthin. Journal ofAtherosclerosis and Thrombosis, 7, 216−222.

Je, J. Y., Park, P. J., & Kim, S. K. (2004). Free radical scavenging properties of hetero-chitooligosaccharides using an ESR spectroscopy. Food and Chemical Toxicology, 42,381−387.

Je, J. Y., Qian, Z. J., Byun, H. G., & Kim, S. K. (2007). Purification and characterization of anantioxidant peptide obtained from tuna backbone protein by enzymatic hydrolysis.Process Biochemistry, 42, 840−846.

Jeon, Y. J., Byun, H. G., & Kim, S. K. (1999). Improvement of functional properties of codframe protein hydrolysates using ultrafiltration membranes. Process Biochemistry,35, 471−478.

Jeon, Y. J., & Kim, S. K. (2000a). Continuous production of chitooligosaccharides using adual reactor system. Process Biochemistry, 35, 623−632.

Jeon, Y. J., & Kim, S. K. (2000b). Production of chitooligosaccharides using ultrafiltrationmembrane reactor and their antibacterial activity. Carbohydrate Polymers, 41,133−141.

Jeon, Y. J., & Kim, S. K. (2002). Antitumor activity of chitosan oligosaccharides produced inultrafiltrationmembrane reactor system. Journal ofMicrobiologyandBiotechnology,12(3),503−507.

Jun, S. Y., Park, P. J., Jung, W. K., & Kim, S. K. (2004). Purification and characterization ofan antioxidative peptide from enzymatic hydrolysate of yellowfin sole (Limandaaspera) frame protein. European Food Research Technology, 219, 20−26.

Jung, W. K., Ahn, Y. W., Lee, S. H., Choi, Y. H., Kim, S. K., Yea, S. S., et al. (2009). Eckloniacava ethanolic extracts inhibit lipopolysaccharide-induced cyclooxygenase-2 andinducible nitric oxide synthase expression in BV2 microglia via the MAP kinase andNF-kB pathways. Food and Chemical Toxicology, 47, 410−417.

Jung, H. A., Hyun, S. K., Kim, H. R., & Choi, J. S. (2006). Angiotensin-converting enzyme Iinhibitory activity of phlorotannins from Ecklonia stolonifera. Fisheries Science, 72,1292−1299.

Jung, W. K., Rajapakse, N., & Kim, S. K. (2005). Antioxidative activity of a low molecularweight peptide derived from the sauce of fermented blue mussel, Mytilus edulis.European Food Research Technology, 220, 535−539.

Kang, K. A., Lee, K. H., Chae, S. W., Koh, Y. S., Yoo, B. S., Kim, J. H., et al. (2005).Triphlorethol-A from Ecklonia cava protects V79-4 lung fibroblast against hydrogenperoxide induced cell damage. Free Radical Research, 39, 883−892.

Kang, K. A., Lee, K. H., Chae, S., Zhang, R., Jung, M. S., Ham, Y. M., et al. (2006).Cytoprotective effect of phloroglucinol on oxidative stress induced cell damage viacatalase activation. Journal of Cellular Biochemistry, 97, 609−620.

Kang, K. A., Lee, K. H., Chae, S., Zhang, R., Jung, M. S., Lee, Y., et al. (2005). Eckol isolatedfrom Ecklonia cava attenuates oxidative stress induced cell damage in lungfibroblast cells. FEBS Letters, 579, 6295−6304.

Kim, S. K., Byun, H. G., Kang, T. J., & Song, D. J. (1993). Enzymatic hydrolysis of yellowfinsole skin gelatin in a continuous hollow fiber membrane reactor. Bulletin of KoreanFisheries Society, 26, 120−132.

Kim, S. H., Choi, D. S., Athukorala, Y., Jeon, Y. J., Senevirathne, M., & Rha, C. K. (2007).Antioxidant activity of sulfated polysaccharides isolated from Sargassum fulvellum.Journal of Food Science and Nutrition, 12, 65−73.

Kim, S. Y., Je, J. Y., & Kim, S. K. (2007). Purification and characterization of antioxidantpeptide from hoki (Johnius balengerii) frame protein by gastrointestinal digestion.Journal of Nutritional Biochemistry, 18, 31−38.

Kim, K. N., Joo, E. S., Kim, K. I., Kim, S. K., Yang, H. P., & Jeon, Y. J. (2005). Effect of chitosanoligosaccharides on cholesterol level and antioxidant enzyme activities inhypercholesterolemic rat. Journal of Korean Society of Food Science and Nutrition,34(1), 36−41.

Kim, S. K., & Mendis, E. (2006). Bioactive compounds from marine processingbyproducts — A review. Food Research International, 39, 383−393.

Kim, S. K., Nghiep, N. D., & Rajapakse, N. (2006). Therapeutic prospectives of chitin,chitosan and their derivatives. Journal of Chitin Chitosan, 11(1), 1−10.

Kim, S. K., & Rajapakse, N. (2005). Enzymatic production and biological activities ofchitosan oligosaccharides (COS): A review. Carbohydrate Polymers, 62, 357−368.

Kim, S. K., & Wijesekara, I. (2010). Development and biological activities of marine-derived bioactive peptides: A review. Journal of Functional Foods, 2, 1−9.

Kobayashi, M., & Sakamoto, Y. (1999). Singlet oxygen quenching ability of astaxanthinesters from the green alga Haematococcus pluvialis. Biotechnology Letters, 21,265−269.

Kong, C. S., Kim, J. A., Yoon, N. Y., & Kim, S. K. (2009). Induction of apoptosis byphloroglucinol derivative from Ecklonia cava in MCF-7 human breast cancer cells.Food and Chemical Toxicology, 47, 1653−1658.

Kristinsson,H. G., & Rasco, B. A. (2000). Fish protein hydrolysates: Production, bio-chemicaland functional properties. Critical Reviews in Food Science and Nutrition, 32, 1−39.

Kurashige, M., Okimasu, E., Inoue, M., & Utsumi, K. (1990). Inhibition of oxidative injuryof biological membranes by astaxanthin. Physiological Chemistry and Physics andMedical NMR, 22, 27−38.

Lee, S. H., Li, Y., Karadeniz, F., Kim, M. M., & Kim, S. K. (2009). α-Glycosidase andα-amylase inhibitory activities of phloroglucinal derivatives from edible marinebrown alga, Ecklonia cava. Journal of Science of Food and Agriculture, 89, 1552−1558.

Leiro, J. M., Castro, R., Arranz, J. A., & Lamas, J. (2007). Immunomodulating activities ofacidic sulphated polysaccharides obtained from the seaweed Ulva rigida C. Agardh.International Immunopharmacology, 7, 879−888.

Li, Y., Qian, Z. J., Ryu, B. M., Lee, S. H., Kim, M. M., & Kim, S. K. (2009). Chemicalcomponents and its antioxidant properties in vitro: An edible marine brown alga,Ecklonia cava. Bioorganic and Medicinal Chemistry, 17, 1963−1973.

Liu, Z., Dong, S., Xu, J., Zeng, M., Song, H., & Zhao, Y. (2008). Production of cysteine-richantimicrobial peptide by digestion of oyster (Crassostrea gigas) with alcalase andbromelin. Food Control, 19, 231−235.

Liu, B., Liu,W. S., Han, B.Q., & Sun, Y. Y. (2007). Antidiabetic effects of chitooligosaccharideson pancreatic islet cells in streptozotocin-induced diabetic rats. World Journal ofGastroenterology, 13(5), 725−731.

Lyons, N. M., & O'Brien, N. M. (2002). Modulatory effects of an algal extract containingastaxanthin on UVA-irradiated cells in culture. Journal of Dermatological Science, 30,73−84.

Mayer, A. M. S., & Hamann, M. T. (2002). Marine Pharmacology in 1999: compoundswith antibacterial, anticoagulant, antifungal, anthelmintic, anti-inflammatory,antiplatelet, antiprotozoal and antiviral activities affecting the cardiovascular,endocrine, immune and nervous systems, and other miscellaneous mechanisms ofaction. Comparative Biochemistry and Physiology Part C, 132, 315−339.

McLellan, D. S., & Jurd, K. M. (1992). Anticoagulants from marine algae. BloodCoagulation and Fibrinolysis, 3, 69−80.

Mendis, E., Rajapakse, N., Byun, H. G., & Kim, S. K. (2005). Investigation of jumbo squid(Dosidicus gigas) skin gelatin peptides for their in vitro antioxidant effects. LifeSciences, 77, 2166−2178.

Mendis, E., Rajapakse, N.,& Kim, S. K. (2005). Antioxidant properties of a radical-scavengingpeptide purified from enzymatically prepared fish skin gelatin hydrolysate. Journal ofAgricultural Food Chemistry, 53, 581−587.

Miki, W. (1991). Biological functions and activities of animal carotenoids. Pure andApplied Chemistry, 63, 141−146.

Miura, T., Usami, M., Tsuura, Y., Ishida, H., & Seino, Y. (1995). Hypoglycemic andhypolipidemic effects of chitosan in normal and neonatal streptozotocin-induceddiabetic mice. Biological and Pharmaceutical Bulletin, 18, 1623−1625.

Miyashita, K., & Hosokawa, M. (2008). Beneficial health effects of seaweed carotenoid,fucoxanthin. In C. Barrow, & F. Shahidi (Eds.), Marine nutraceuticals and functionalfoods (pp. 297−319). Boca Raton, FL: CRC Press/Taylor & Francis Group.

Moller, N. P., Scholz-Ahrens, K. E., Roos, N., & Schrezenmeir, J. (2008). Bioactive peptidesand proteins from foods: Indication for health effects. European Journal of Nutrition,47, 171−182.

Mourao, P. A. (2007). A carbohydrate-based mechanism of species recognition in seaurchin fertilization. Brazilian Journal of Medical and Biological Research, 40, 5−17.

Mourao, P. A. S., & Pereira, M. S. (1999). Searching alternatives for heparin: Sulfatedfucans from marine invertebrates. Trends in Cardiovascular Medicine, 9, 225−232.

Nagai, T., & Suzuki, N. (2000). Isolation of collagen from fish waste material — Skin,bone, and fins. Food Chemistry, 68, 277−281.

Nagayama, K., Iwamura, Y., Shibata, T., Hirayama, I., & Nakamura, T. (2002). Bactericidalactivity of phlorotannins from the brown alga Ecklonia kurome. Journal ofAntimicrobial Chemotherapy, 50, 889−893.

Ngo, D. N., Lee, S. H., Kim, M. M., & Kim, S. K. (2009). Production of chitinoligosaccharides with different molecular weights and their antioxidant effect inRAW 264.7 cells. Journal of Functional Foods, 1, 188−198.

Nishida, Y., Yamashita, E., & Miki, W. (2007). Quenching activities of common hydrophilicand lipophilic antioxidants against singlet oxygenusing chemiluminescencedetectionsystem. Carotenoid Science, 11, 16−20.

Palozza, P., & Krinsky, N. (1992). Astaxanthin and canthaxanthin are potent antioxidantin a membrane model. Archives of Biochemistry and Biophysics, 297, 291−295.

Park, P. J., Je, J. Y., & Kim, S. K. (2003). Free radical scavenging activity ofchitooligosaccharides by electron spin resonance spectrometry. Journal of Agriculturaland Food Chemistry, 51, 4624−4627.

Park, P. J., Jung, W. K., Nam, K. D., Shahidi, F., & Kim, S. K. (2001). Purification andcharacterization of antioxidative peptides from protein hydrolysate of lecithin-freeegg yolk. Journal of American Oil Chemists Society, 78, 651−656.

Park, P. J., Lee, H. K., & Kim, S. K. (2004). Preparation of hetero-chitooligosaccharides andtheir antimicrobial activity on Vibrio parahaemolyticus. Journal of Microbiology andBiotechnology, 14(1), 41−47.

Penta-Ramos, E. A., & Xiong, Y. L. (2001). Antioxidative activity of whey proteinhydrolysates in a liposomal system. Journal of Dairy Science, 84, 2577−2583.

Pihlanto-Leppala, A. (2001). Bioactive peptides derived from bovine proteins: Opioidand ACE-inhibitory peptides. Trends in Food Science and Technology, 11, 347−356.

Qi, H., Zhang, Q., Zhao, T., Chen, R., Zhang, H., Niu, X., et al. (2005). Antioxidant activity ofdifferent sulfate content derivatives of polysaccharide extracted from Ulva pertusa(Chlorophyta) invitro. International Journal ofBiologicalMacromolecules,37, 195−199.

Qian, Z. J., Jung, W. K., Byun, H. G., & Kim, S. K. (2008). Protective effect of anantioxidative peptide purified from gastrointestinal digests of oyster, Crassostreagigas against free radical induced DNA damage. Bioresource Technology, 99,3365−3371.

Ragan, M. A., & Glombitza, K. W. (1986). Handbook of physiological methods(pp. 129−241). Cambridge: Cambridge University Press.

Rajapakse, N., Jung, W. K., Mendis, E., Moon, S. H., & Kim, S. K. (2005). A novelanticoagulant purified from fish protein hydrolysate inhibits factor XIIa and plateletaggregation. Life Sciences, 76, 2607−2619.

Rajapakse, N., Kim, M. M., Mendis, E., & Kim, S. K. (2007). Inhibition of free radical-mediated oxidation of cellular biomolecules by carboxylated chitooligosaccharides.Bioorganic and Medicinal Chemistry, 15, 997−1003.

Ranathunga, S., Rajapakse, N., & Kim, S. K. (2006). Purification and characterization ofantioxidative peptide derived from muscle of conger eel (Conger myriaster).European Food Research Technology, 222, 310−315.

Rao, A. V., & Rao, L. G. (2007). Carotenoids and human health. Pharmacological Research,55, 207−216.

Rocha de Souza,M. C., Marques, C. T., Dore, C.M. G., Ferreira da Silva, F. R., Rocha, H. A. O., &Leite, E. L. (2007). Antioxidant activities of sulphated polysaccharides frombrown andred seaweeds. Journal of Applied Phycology, 19, 153−160.

529D.-H. Ngo et al. / Food Research International 44 (2011) 523–529

Rocha, H. A., Franco, C. R., Trindade, E. S., Veiga, S. S., Leite, E. L., Nader, H. B., et al. (2005).Fucan inhibits Chinese hamster ovary cell (CHO) adhesion to fibronectin by bindingto the extracellular matrix. Planta Medica, 71, 628−633.

Ruperez, P. (2001). Antioxidant activity of sulphated polysaccharides from the Spanishmarine seaweed Nori. Proceedings of the COST 916 European conference on bioactivecompounds in plants foods (pp. 114). Tenerife, Canary Islands, Spain: Health Effectsand Perspectives for the Food Industry.

Ruperez, P., Ahrazem, O., & Leal, A. (2002). Potential antioxidant capacity of sulphatedpolysaccharides from the edible marine brown seaweed Fucus vesiculosus. Journalof Agricultural and Food Chemistry, 50, 840−845.

Sachindra, N. M., Sato, E., Maeda, H., Hosokawa, M., Niwano, Y., Kohno, M., et al. (2007).Radical scavenging and singlet oxygen quenching activity of marine carotenoidfucoxanthin and its metabolites. Journal of Agricultural and Food Chemistry, 55,8516−8522.

Schaeffer, D. J., & Krylov, V. S. (2000). Anti-HIV activity of extracts and compounds fromalgae and cyanobacteria. Ecotoxicology and Environmental Safety, 45, 208−227.

Shahidi, F. (2007). Maximising the value of marine by-products. Florida, USA: CRC Press.Shahidi, F., Han, X. Q., & Synowiecki, J. (1995). Production and characteristics of protein

hydrolysates from capelin (Mallotus villosus). Food Chemistry, 53, 285−293.Shahidi, F., & Zhong, Y. (2008). Bioactive peptides. Journal of AOAC International, 91,

914−931.Sheih, I. C., Wu, T. K., & Fang, T. J. (2009). Antioxidant properties of a new antioxidative

peptide from algae protein waste hydrolysate in different oxidation systems.Bioresource Technology, 100, 3419−3425.

Shibata, T., Ishimaru, K., Kawaguchi, S., Yoshikawa, H., & Hama, Y. (2008). Antioxidantactivities of phlorotannins isolated from Japanese Laminariaceae. Journal of AppliedPhycology, 20, 705−711.

Simpson, B. K. (2007). Pigments fromby-products of seafood processing. In F. Shahidi (Ed.),Maximising the value of marine by-products (pp. 413−432). Boca Raton, Cambridge:CRC Press/Woodhead Publishing Ltd.

Stahl, W., & Sies, H. (1996). Lycopene: A biologically important carotenoid for humans?Archives of Biochemistry and Biophysics, 336, 1−9.

Sun, L., Wang, C., Shi, Q., & Ma, C. (2009). Preparation of different molecular weightpolysaccharides from Porphyridium cruentum and their antioxidant activities.International Journal of Biological Macromolecules, 45, 42−47.

Turujman, S. A., Wamer, W. G., Wei, R. R., & Albert, R. H. (1997). Rapid liquidchromatographic method to distinguish wild salmon from aquacultured salmonfed synthetic astaxanthin. Journal of AOAC International, 80, 622−632.

Wang, J., Zhang, Q., Zhang, Z., & Li, Z. (2008). Antioxidant activity of sulphatedpolysaccharide fractions extracted from Laminaria japonica. International Journal ofBiological Macromolecules, 42, 127−132.

Wijesekara, I., Yoon, N. Y., & Kim, S. K. (2010). Phlorotannins from Ecklonia cava(Phaeophyceae): Biological activities and potential health benefits. Biofactors, 36,408−414.

Xia, W., Liu, P., Zhang, J., & Chen, J. (2010). Biological activities of chitosan andchitooligosaccharides. Food Hydrocolloids, 25, 170−179.

Xue, C., Yu, G., Hirata, T., Terao, J., & Lin, H. (1998). Antioxidative activities of severalmarine polysaccharides evaluated in a phosphatidylcholine-liposomal suspensionand organic solvents. Bioscience, Biotechnology and Biochemistry, 62, 206−209.

Yan, X. J., Chuda, Y., Suzuki, M., & Nagata, T. (1999). Fucoxanthin as themajor antioxidant inHizikia fusiformis, a commonedible seaweed. Bioscience, Biotechnology and Biochemistry,63(3), 605−607.

Yang, C. S., Landau, J. M., Huang, M. T., & Newmark, H. L. (2001). Inhibition ofcarcinogenesis by dietary polyphenolic compounds. Annual Reviews in Nutrition, 21,381−406.

Yokoyama, K., Chiba, H., & Yoshikawa, M. (1992). Peptide inhibitors for angiotensin I-converting enzyme from thermolysin digest of dried bonito. Bioscience Biotechnologyand Biochemistry, 56, 1541−1545.

Yoon, N. Y., Lee, S. H., Li, Y., & Kim, S. K. (2009). Phlorotannins from Ishige okamurae andtheir acetyl- and butyry-lcholinesterase inhibitory effects. Journal of FunctionalFoods, 1, 331−335.

Yoon, N. Y., Ngo, D. N., & Kim, S. K. (2009). Acetylcholinesterase inhibitory of novelchitooligosaccharide derivatives. Carbohydrate Polymers, 78, 869−872.

Zhang, R., Kang, K. A., Piao, M. J., Ko, D. O., Wang, Z. H., Lee, I. K., et al. (2008). Eckolprotects V79-4 lung fibroblast cells against ύ-ray radiation-induced apoptosis viathe scavenging of reactive oxygen species and inhibiting of the c-Jun NH2-terminalkinase pathway. European Journal of Pharmacology, 591, 114−123.

Zhang, Q., Li, N., Zhou, G., Lu, X., Xu, Z., & Li, Z. (2003). In vivo antioxidant activity ofpolysaccharide fraction from Porphyra haitanensis (Rhodephyta) in aging mice.Pharmacological Research, 48, 151−155.