Food Chemistry 275 (2019) 644–660

Contents lists available at ScienceDirect

Food Chemistry
journal homepage: www.elsevier.com/locate/foodchem

Review

The Maillard reaction products as food-born antioxidant and antibrowning T

agents in model and real food systems
⁎
Majid Nooshkam, Mehdi Varidi , Moein Bashash
Department of Food Science and Technology, Faculty of Agriculture, Ferdowsi University of Mashhad (FUM), Mashhad, Iran

A R T I C LE I N FO A B S T R A C T

Keywords: Food products containing lipids, especially unsaturated fatty acids, are prone to oxidation reactions, which lead
Lipid oxidation to the formation of off-flavor, due to side-reaction products that potentially have toxic effects and reduce shelf-
Maillard reaction life. The Maillard reaction products (MRPs) are widely produced in foods containing reducing sugars and amino-
Maillard reaction products bearing compounds during thermal processing and storage. MRPs possess excellent antioxidant ability in many
Antioxidant mechanism
food products, through chelation of metal ions, breakdown of radical chains and hydrogen peroxide, and
Antibrowning
scavenging of reactive oxygen species. This review presents an overview of the antioxidant activity of MRPs in
Free radicals
Reducing capacity model and real food systems. It also provides the pros and cons of the Maillard reaction, some available anti-
Metal chelation oxidant assays to evaluate the antioxidative ability of MRPs, and parameters influencing their functional
properties. In addition, metal chelation-based antibrowning ability of MRPs to inhibit the enzymatic browning
reaction in fruits and vegetables is discussed.

1. Introduction
Lipids are recognized as an important food component with diverse
roles. For instance, they act as a storage source of energy, a medium to
amplify the rate of heat transfer, and give appropriate texture, flavor,
and nutritional properties to food products (Shahidi & Zhong, 2010).
However, lipid oxidation results in off-flavors and side-reaction pro-
ducts with potentially toxic activities in the food sector, which may
damage nutritional value or even create some diseases related to the
peroxidation-derived components (Zhong et al., 2015). Synthetic (bu-
tylated hydroxytoluene (BHT), butylated hydroxyanisole (BHA), and
tert-butyl hydroquinone (TBHQ)) and natural antioxidants are the main
compounds applied to inhibit the oxidation reaction of lipids via ter-
minating radical chain reactions. However, there is concern about the
use of the synthetic antioxidants due to their possible toxic effects on
human health (Shahidi, 2000). In addition, natural antioxidants have
higher cost compared to synthetic ones and, therefore, many attempts
have been made to boost their efficacy (Chang, Lee, & Lee, 2005). The
Maillard reaction products (MRPs) that are widely produced during the
thermal processing and storage of foods, can be used as normal, natural,
and endogenous antioxidants to delay or inhibit the oxidation reaction
of food lipids. The Maillard reaction produces some products, such as
melanoidins and Amadori rearrangement products (ARPs), with po-
tential to chelate metals and scavenge oxygen radicals. Another specific
feature is polyphenol oxidase (PPO) inhibitory effect, which may pre-
vent enzymatic browning in fruits and vegetables (Yuan et al., 2015).
The present review highlights the antioxidant and antibrowning activ-
ities of MRPs in model and real food systems. Additionally, the pros and

Abbreviations: AAPH, 2,2′-azobis(2-amidinopropane) dihydrochloride; XTT, 2,3-bis(2-methoxy-4-nitro-5-sulfophenyl)-2H-tetrazolium-5-carboxanilide; ABTS, 2,2′-

azinobis(3-ethylbenzothiazoline-6-sulphonic acid) diammonium salt; ABAP, 2,2′-azobis(2-methylpropionamidine) dihydrochloride; DPPH, 2,2-diphenyl-1-pi-
crylhydrazyl or 1,1-diphenyl-2-picrylhydrazyl; HMFone, 4-hydroxy-5-methyl-2,3-dihydrofuran-3-one; Abs 420 nm, absorbance at 420 nm; Abs 294 nm, absorbance at
294 nm; ABTS-RS, ABTS radical scavenging; AGEs, Advanced glycation end-products; ARPs, Amadori rearrangement products; ACE, Angiotensin converting enzyme;
BSA, Bovine serum albumin; BHA, butylated hydroxyanisole; BHT, butylated hydroxytoluene; DPPH-RS, DPPH radical scavenging; FRAP, ferric reducing/antioxidant
power; HAHp, half-fin anchovy hydrolysates; HRPs, Heyns rearrangement products; HMW, high molecular weight; HAT, hydrogen atom transfer; HR, hydroxyl
radical; HRS, hydroxyl radical scavenging; LMW, low molecular weight; MRPs, Maillard reaction products; MDA, Malondialdehyde; CML, N∊ (carboxymethyl)lysine;
OVA, ovalbumin; ORAC, oxygen radical absorbing capacity; POD, peroxidase; PR, peroxyl radical; PRS, peroxyl radical scavenging; PPO, polyphenol oxidase; PUFA,
polyunsaturated fatty acids; PPP, porcine plasma protein; PGR, pyrogallol red; RH, relative humidity; SDS, sodium dodecyl sulfate; SAS, superoxide anion scavenging;
TBHQ, tert-butyl hydroquinone; TBA, thiobarbituric acid; TBARS, thiobarbituric acid reactive substances; UV, ultraviolet; aw, water activity; WPH, whey protein
hydrolysate; WPI, whey protein isolate; α-LA, α-lactalbumin; β-LG, β-lactoglobulin
⁎
Corresponding author.
E-mail address: m.varidi@um.ac.ir (M. Varidi).

https://doi.org/10.1016/j.foodchem.2018.09.083
Received 16 May 2018; Received in revised form 10 September 2018; Accepted 12 September 2018
Available online 14 September 2018
0308-8146/ © 2018 Elsevier Ltd. All rights reserved.
M. Nooshkam et al.
Fig. 1. The Hodge diagram; designed with respect to Martins et al. (2000).
cons of the Maillard reaction, antioxidant assays, and factors influen-
cing the antioxidant activity of MRPs are discussed.
2. Overview of the Maillard reaction
The Maillard reaction is a chemical and non-enzymatic browning
reaction that initiates through conjugation of compounds bearing free
amino and carbonyl groups during the thermal processing and storage
of foods (Wang, Qian, & Yao, 2011). Browning reaction at controlled
levels plays an important role in developing desirable sensory attributes
like colors, aromas, and flavors in some foods, such as bread, baked
products, and roasted coffee and nuts. It is generally agreed that the
average human diet contains a significant amount of MRPs (O’Brien,
Morrissey, & Ames, 1989; Rufian-Henares & De la Cueva, 2008;
Pastoriza & Rufián-Henares, 2014). Additionally, diverse reaction pro-
ducts from the Maillard reaction may alter nutritional value of foods by
reducing the digestibility of proteins and generating some toxic and
mutagenic compounds, but antioxidant products can also be formed
(Martins, Jongen, & van Boekel, 2000).
The Maillard reaction comprises three steps, including early, inter-
mediate, and final stages (Fig. 1). In the initial stage, a Schiff base is
formed through the reaction of active carbonyl moiety of a reducing
sugar, oxidized lipid or vitamin C with free amino group of a protein,
peptide or free amino acid concomitant with water molecule release.
Afterwards, Schiff base cyclization leads to the formation of a low
stability N-substituted glycosylamine as a condensation product. This is
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Food Chemistry 275 (2019) 644–660
the only reversible step of the Maillard reaction (O’Brien et al., 1989).
The glycosylamine is then rearranged to more stable early MRPs, i.e.,
Amadori rearrangement products (ARPs, 1-amino-1-deoxy-2-ketose
from aldose sugars) or Heyns rearrangement products (HRPs, 2-amino-
2-deoxyaldose from ketose sugars) (de Oliveira, Coimbra, de Oliveira,
Zuñiga, & Rojas, 2016). This is the first irreversible step of the non-
enzymatic glycation reaction and results in an increase in reducing
power (likely due to the increased number of hydroxyl groups provided
by conjugation) and decrease in the biological value of proteins (due to
a decrease in nutritional availability of essential amino acids). How-
ever, there is no change in color, flavor or off-flavor, fluorescence,
toxicity, and solubility of the rearrangement products (Nursten, 2005).
Subsequently, ARPs and likely HRPs degrade to intermediate com-
pounds according to the pH value of the reaction medium and two
routes of 1,2-enolization and 2,3-enolization can be observed. The
former is performed at pH values ≤7.0 and the corresponding products
are hydroxymethylfurfural (from hexoses) or furfural (from pentoses),
while the latter is dominant at basic pH values and the corresponding
degradation products from ARPs are reductones (e.g., 4-hydroxy-5-
methyl-2,3-dihydrofuran-3-one (HMFone)) and fission products (e.g.,
acetol, diacetyl, and pyruvaldehyde) (Martins et al., 2000). The main
characteristics of the intermediate stage are production of formic and
acetic acids, yellowish color, fluorescence, flavor or off-flavor, carbon
dioxide, increase in reducing power, and strong absorption in the near-
ultraviolet (near-UV) region (Nursten, 2005; Karbasi & Madadlou,
2018; Martins et al., 2000). The UV absorbance value at 294 nm (Abs
M. Nooshkam et al.
294 nm) can be used to evaluate the amount of intermediate MRPs
(Nooshkam & Madadlou, 2016a,b).
In the final stage of the Maillard reaction, aldol and aldehyde-amine
condensations of reductones, fission products, and Strecker degradation
products lead to the formation of brown, nitrogen-containing polymers
(3–4% N), and macromolecular materials called melanoidins (Nursten,
2005; Peng, Ma, Chen, & Wang, 2011) with maximum absorbance at
420 nm (Abs 420 nm) (Vhangani & Van Wyk, 2013). The molecular
weight of MRPs, especially melanoidins, is significantly dependent on
thermal intensity; the Maillard reaction at initial stages forms low
molecular weight (LMW) MRPs and longer reaction periods (more than
24 h) lead to the creation of high molecular weight (HMW) melanoi-
dins. The Maillard reaction in actual foods predominantly produces
HMW melanoidins (e.g., > 5 kDa in roasted cocoa beans, > 12 kDa in
sweet wines, > 12–14 kDa in coffee, and > 60 kDa in roasted malt)
(Wang et al., 2011). Food melanoidins are anionic chromophoric
compounds with functionalities including antioxidative, antimicrobial,
prebiotic, and antihypertensive activities (Rufián-Henares & Morales,
2007b). Several compounds, such as furans, pyrroles, pyridines, pyr-
azines, and carbonyl components, were detected in melanoidins iso-
lated from model and some real food systems (Wang et al., 2011).
Melanoidins are found in large amounts in cooked, fried, and roasted
foods, which are consumed daily (Pastoriza & Rufián-Henares, 2014).
3. Pros and cons of the Maillard reaction
The Maillard reaction is responsible for a distinct aroma, flavor, and
special palatability of foods like bread, pizza, roasted peanut, coffee,
barbecued beef roast, flamed chicken, and beer. It also improves anti-
oxidant activity of food products (Losso, 2016). This non-enzymatic
browning reaction has been extensively applied to increase surface-
active properties of proteins via tuning hydrophilic-hydrophobic bal-
ances and providing a continuous thick and viscoelastic layer at air/
water or oil/water interfaces (De Oliveira et al., 2016; Nooshkam &
Madadlou, 2016b), as well as to improve their solubility and stability
over a wide range of temperature and pH value (Han, Yi, Wang, &
Huang, 2017; Perusko, Al-Hanish, Velickovic, & Stanic-Vucinic, 2015).
The Maillard reaction also forms melanoidins with antimicrobial and
antioxidant abilities (Hamdani, Wani, Bhat, & Siddiqi, 2018). However,
some undesirable properties and health-related issues are observed in
this reaction. It was reported that the Maillard reaction led to color loss
along with product darkening (at uncontrolled conditions), lysine loss,
and the generation of pyridines, furans, and mutagenic compounds as
well as advanced glycation end-products (AGEs) (Losso, 2016).
Several AGEs, such as pentosidine, crossline, N∊ (carboxymethyl)
lysine (CML), pyrraline, furosine, and imidazolones can be formed by
further rearrangement, oxidation, and reduction of the early MRPs (Van
Nguyen, 2006). Up to now, the chemical structure of more than 20
AGEs has been characterized mainly in baked or roasted foods like
peanut and sterilized products such as enteral formulas (Gupta et al.,
2018; Rufián-Henares, Guerra-Hernández, & García-Villanova, 2004).
Some documents have shown that AGEs, especially dietary ones are
related to oxidant stress and inflammation and subsequently diabetes
and cardiovascular diseases (Van Nguyen, 2006; Silván, Assar, Srey, Del
Castillo, & Ames, 2011). Additionally, AGEs contribute in food allergy
and their high intake amounts may result in remarkable cellular dys-
function, such as modification of protein structures and lipid metabo-
lism interference along with vascular inflammation and thrombogenesis
(Gupta et al., 2018).
A daily intake of 25–75 mg has been reported for AGEs CML and
pyrraline in a regular Western diet (Schwarzenbolz, Hofmann,
Sparmann, & Henle, 2016). It is worth mentioning that HMW AGEs
have a slower absorption rate and less efficient absorption than LMW
counterparts. HMW AGEs can be partially degraded by gut proteases
and their bioavailability will depend on the diet type, gut environment,
associated peptide size, and resident time in the gut (Poulsen et al.,
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Food Chemistry 275 (2019) 644–660
2013). There are several synthetic carbonyl scavengers (e.g., amino-
guanidine and pyridoxamine) and natural AGE inhibitors (e.g., phenolic
compounds and plant extracts) to inhibit the formation of AGEs (Peng
et al., 2011). Silván et al. (2011) successfully used ferulic acid as a
natural polyphenol for inhibiting AGE formation and reported that
ferulic acid decreased the CML and fluorescent AGEs (about 90%), but
early MRPs and melanoidins were inhibited to a lesser extent (10% and
28%, respectively). They also stated that AGEs are mainly formed at
high temperatures under alkaline and oxidative conditions.
In addition, dry heating promotes the formation of new dietary
AGEs by 10- to 100-fold higher than the uncooked state. For example,
animal-derived foods which contain high levels of fat and protein are
prone to generate new AGEs during cooking and they are rich sources of
AGEs (Uribarri et al., 2010). Foods with high lipid contents may un-
dergo oxidation reaction during various cooking methods to form oxi-
dation products such as aldehydes and ketones (Domínguez, Gómez,
Fonseca, & Lorenzo, 2014), which can contribute to the Maillard re-
action as carbonyl sources. Conversely, foods that are rich in carbo-
hydrates, such as vegetables, fruits, low-fat milk, and whole grains, are
relatively low in AGEs even after cooking. This was attributed to the
high water content, vitamins, antioxidants, and non-reducing poly-
saccharides in these foods, which can lower AGEs (Uribarri et al.,
2010). It can be concluded that the generation of new dietary AGEs can
be prevented during cooking by the use of AGE-inhibitory compounds
such as aminoguanidine and also reduced significantly through wet-
heating process at lower temperatures and shorter times or even by
using acidic ingredients like lemon juice or vinegar (Uribarri et al.,
2010). In this way, the reaction rate and, in turn, AGEs formation is
decreased via rising water content and lowering pH value, temperature,
and time along with the addition of AGE inhibitors.
Currently, many researches have focused on the potential use of
early MRPs and melanoidins as functional food ingredients (Jiang, Rai,
O’Connor, & Brodkorb, 2013; Jiménez-Zamora, Pastoriza, & Rufián-
Henares, 2015; Nooshkam, Babazadeh, & Jooyandeh, 2018; Vhangani
& Van Wyk, 2013). It is noteworthy that the highly glycated proteins
through the Maillard reaction show lower safety issues in comparison
with chemically modified proteins and, therefore, can be used as
functional food ingredients to ameliorate nutritional, textural, and
sensorial properties of food products (de Oliveira et al., 2016). In
general, it can be deduced that the Maillard reaction should be mon-
itored under controlled reaction conditions to acquire MRPs with the
optimum technological functionality and antioxidation. Furthermore,
bioactive melanoidins can be separated and purified by means of sev-
eral membrane and dialyzing techniques to be used as potentially
functional supplement in food products.
4. Antioxidant activity of MRPs
The antioxidant properties of some compounds produced during the
progress of the Maillard reaction or heating of reducing sugars, i.e.,
caramelization products, Amadori compounds, reactive reductones,
premelanoidins, and melanoidins, have been reported in processed
foods (Billaud, Roux, Brun-Merimee, Maraschin, & Nicolas, 2003). The
antioxidative activity of MRPs in model and food systems is due to
different antioxidant mechanisms, including chelation of metal ions,
radical chains breaking, breakdown of hydrogen peroxide, and
scavenging of reactive oxygen species (Nooshkam & Madadlou, 2016a).
4.1. Methods used to evaluate antioxidant activity of MRPs
Different antioxidant assays used to characterize the antioxidative
attributes of MRPs, their prevailing conditions, and proposed mechan-
isms are shown in Table 1.
4.1.1. Reducing capacity
Reducing power and ferric reducing/antioxidant power (FRAP)
 M. Nooshkam et al.

Table 1
Antioxidative assays used for evaluating the antioxidant activity of Maillard reaction products (MRPs).
Antioxidant assay Reagents Incubation time Incubation Wavelength (nm) Reaction mechanisms Reference
(min) Temp (°C)

Reducing power Potassium ferricyanide; trichloroacetic 20 50 700 Reducing activity of hydroxyl groups Vhangani and Van Wyk (2013), Jiang et al.
acid; ferric chloride of MRPs via their redox potential of (2013), Wang et al. (2013), Khadidja et al.
transferring electrons (2017), Hamdani et al. (2018)
Hydrogen atom donation
DPPH-RS activity DPPH; ethanol or methanol 30 25 517 Hydrogen donation Jiang and Brodkorb (2012), Benjakul et al.
(2005), Yan et al. (2018)
ABTS-RS activity ABTS; potassium persulfate 2–6 25 734 Direct reduction via electron transfer Kim and Lee (2009), Sun, Hayakawa,
Radical quenching via hydrogen Chuamanochan, et al. (2006), Sun, Hayakawa,
atom transfer Puangmanee, et al. (2006), Sun et al. (2004)
FRAP FRAP reagent (TPTZ (2,4,6-tripyridyl-s- 30 37 595 Radical chain breaking by donation Kim and Lee (2009), Karnjanapratum et al.
triazine), HCl, FeCl3, acetate buffer) of a hydrogen atom (2017)
Reducing activity of hydroxyl groups
PRS activity PGR; ABAP 120 37 540 Hydrogen atom transfer Vhangani and Van Wyk (2013)

647
HRS activity Sodium phosphate buffer; 60 37 536 Prolong the Fenton reaction through Nie et al. (2017)
phenanthroline; ferrous sulfate; hydrogen chelation of the metal ions
peroxide
Chelating activity on ferrous ion FeCl2; ferrozine 10 25 562 Reducing activity of hydroxyl and Gu et al. (2010), Wang et al. (2011)
pyrrole groups
Chelating activity of melanoidins
Superoxide anion scavenging Nitroblue tetrazolium; nicotinamide 5 25 560 Scavenging hydroxyl and superoxide Rao et al. (2011)
activity adenine dinucleotide reduced (NADH); anion radicals
phenazine; methosulfate
Antioxidant activity in SDS/ SDS; linoleic acid; AAPH 90 50 234 Inhibitory activity against formation Sun, Hayakawa, Chuamanochan, et al. (2006),
linoleic acid-AAPH system of conjugated dienes Sun, Hayakawa, Puangmanee, et al. (2006)
β-carotenebleaching assay Linoleic acid; β-carotene; Tween 80; 120 50 470 Free radical-mediated phenomenon Rao et al. (2011)
chloroform
ORAC Fluoresecein; AAPH 15 37 Excitation = 485, Scavenging oxygen radicals Kitts and Hu (2005), Su et al. (2011)
Emission = 527
Tetrazolium salt XTT reducibility XTT solution (containing menadione) 20 25 490 and 570* XTT reduction to formazan Sun et al. (2004)

* Absorbance between 490 and 570 nm (as the reference).

Food Chemistry 275 (2019) 644–660
M. Nooshkam et al.
have been used to determine antioxidant effect of MRPs. Reducing
power is a good index for antioxidant activity of food components. In
this assay the ferric chloride/ferricyanide complex is reduced to ferrous
form (Fe2+) in the presence of antioxidants and therefore the Fe2+
concentration can be monitored spectrophotometrically by measure-
ment of Perl’s Prussian blue color produced at 700 nm (Khadidja, Asma,
Mahmoud, & Meriem, 2017; Vhangani & Van Wyk, 2013). Reducing
power of MRPs is expressed as absorbance units. The assay is frequently
used for evaluating the antioxidative activity of Maillard-type con-
jugates (Lertittikul, Benjakul, & Tanaka, 2007; Wang, Bao, & Chen,
2013). The hydroxyl and pyrrole groups of MRPs play a key role in the
reducing activity of the components via their redox potential of trans-
ferring electrons (Jiang et al., 2013; Vhangani & Van Wyk, 2013). The
radical chain-breaking activity of the intermediate reductone com-
pounds of MRPs through donation of a hydrogen atom has also been
reported as another possible antioxidative mechanism of MRPs (Wang
et al., 2013). The Maillard reaction forms products with boosted re-
ducing power; HMW melanoidins (> 50 kDa) and high concentrations
of MRPs render greater reducing power (Gu et al., 2009; Gu et al.,
2010). By conjugating lysozyme with guar gum, Hamdani et al. (2018)
hypothesized that the higher reducing power of conjugated lysozyme
compared to its unconjugated counterpart is probably due to (i) the
exposure of electron donating amino acid residues (i.e., methionine,
tyrosine, lysine, tryptophan, and cysteine) upon lysozyme denaturation
under alkaline conditions and (ii) higher electron donating ability of the
obtained conjugates, probably through their hydroxyl and pyrrole
groups.
The FRAP assay is a routine antioxidative activity method for
evaluating single antioxidants and total antioxidative activity based on
the ferric iron (Fe3+) reduction to Fe2+ (Kim & Lee, 2009). Hetero-
cyclic products obtained during the Maillard reaction and the thermo-
lysis of Amadori products render reducing activity against ferric ion.
MRPs can act as electron donors and their hydroxyl groups reducing
activity in conjugation with radical chain-breaking effect of inter-
mediate reductone compounds through donation of hydrogen atom
have been reported in the literature (Karnjanapratum, Benjakul, &
O’Brien, 2017; Vhangani & Van Wyk, 2016; Wang et al., 2013).
4.1.2. DPPH-radical scavenging (DPPH-RS) activity
DPPH (2,2-diphenyl-1-picrylhydrazyl or 1,1-diphenyl-2-picrylhy-
drazyl) is a chemical compound with chromogen-radical structure;
antioxidant compounds scavenge the DPPH% to a stable DPPH-H mo-
lecule via the donation of hydrogen concomitant with a color change
from purple to yellow, which can be monitored spectrophotometrically
at 517 nm (Rao, Chawla, Chander, & Sharma, 2011). MRPs obtained
from α-lactalbumin (α-LA)–ribose and β-lactoglobulin (β-LG)–ribose
(Jiang & Brodkorb, 2012), casein–glucose (Gu et al., 2009), irradiated
chitosan–glucose (Rao et al., 2011), whey protein isolate (WPI)/whey
protein hydrolysate (WPH)-lactose/lactulose (Nooshkam & Madadlou,
2016a,b), and bovine serum albumin (BSA) -maltodextrin
(Nasrollahzadeh, Varidi, Koocheki, & Hadizadeh, 2017) exhibited high
DPPH-RS activity. Nasrollahzadeh et al. (2017) demonstrated that hy-
drophobic patches (due to protein ornamentation upon heating) in
molecules tend to interact with hydrophobic radicals such as DPPH,
thereby increasing DPPH-RS ability. They also reported that melanoi-
dins obtained at the final stage of the reaction can function as potent
antioxidants and suppress free radicals. Khadidja et al. (2017) declared
that outstanding DPPH-RS activity of alginate-gelatin MRPs could be
attributed to the hydrogen donating tendency of intermediate or final
products of the Maillard reaction. A similar explanation was reported
by Yan, Yu, and Jing (2018) working on MRPs between chit-
ooligosaccharide and glycine.
4.1.3. ABTS-radical scavenging (ABTS-RS) activity
This assay is based on the direct oxidation of ABTS (2,2′-azinobis(3-
ethylbenzothiazoline-6-sulphonic acid) diammonium salt) with
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Food Chemistry 275 (2019) 644–660
potassium persulfate (K2S2O8) yielding a stable free radical cation
(ABTS%+). The blue-green color of ABTS%+ solution is decolorized in
the presence of antioxidants and the decolorization (reduction) is
evaluated spectrophotometrically by monitoring its absorbance decre-
ment at 734 nm (Kim & Lee, 2009; Sun, Hayakawa, Chuamanochan,
et al., 2006). The direct reduction through electron transfer and radical
quenching via hydrogen atom transfer (HAT) are documented me-
chanisms of antioxidant compounds, which are able to scavenge ABTS
radicals (Kim & Lee, 2009). ABTS-RS activity of MRPs is expressed as
μmol Trolox (a water-soluble vitamin E analogue) equivalent per mL
sample by comparing their percent of inhibition with that of Trolox
(Sun, Hayakawa, Puangmanee, & Izumori, 2006). MRPs obtained from
aqueous glucose/glycine, diglycine, and triglycine model systems (Kim
& Lee, 2009) and egg white glycated with D-psicose, D-fructose, and D-
glucose (Sun, Hayakawa, & Izumori, 2004) showed ABTS-RS activity
mainly because of hydrogen-donating capacity of intermediate or final
brownish compounds (Liu, Li, Kong, Jia, & Li, 2014). It was shown that
MRPs can interact more efficiently with hydrophilic radicals such as
ABTS% and %OH than hydrophobic ones like DPPH% in aqueous solutions
and, therefore, DPPH-RS activity was mainly observed in the early
MRPs, compared to brown pigments which are produced afterwards
(Liu et al., 2014).
4.1.4. Peroxyl radical scavenging (PRS) activity
The reactivity of potential antioxidants against free radicals can be
evaluated by competitive techniques, such as PRS activity assay based
on the HAT mechanism. In this assay, 2,2′-azobis(2-methylpropiona-
midine) dihydrochloride (ABAP), as a water-soluble radical initiator, is
decomposed spontaneously at 37 °C and two carbon-centered free ra-
dicals are formed, which in turn react with oxygen to form peroxyl
radical (PR). The formed PR can oxidize pyrogallol red (PGR) solution
and decrease its color. The ability of MRPs to scavenge PRs has been
reported and they are recognized as potent chain-breaking antioxidants
(Vhangani & Van Wyk, 2013). It is established that PRS activity has a
strong linear relationship with the progress of the Maillard reaction and
the produced melanoidins have significantly high PRS activity (Gómez-
Ruiz, Ames, & Leake, 2008), since these compounds possess the ten-
dency to trap free radicals, scavenge reactive oxygen species, and
chelate metal ions (Mengíbar, Miralles, & Heras, 2017).
4.1.5. Hydroxyl radical scavenging (HRS) activity
Hydroxyl radical (HR) is produced through the Fenton reaction
(Fe2+ + H2O2 → Fe3+ + OH− + %OH) when hydrogen peroxide is
present in a system (Yen & Hsieh, 1995). HR oxidizes deoxyribose to
malondialdehyde (MDA), from which a pink chromagen with maximum
absorbance at 532 nm is produced via the reaction of MDA with thio-
barbituric acid (TBA). Antioxidants such as MRPs suppress mal-
ondialdehyde formation through scavenging the HR by competing with
deoxyribose (Vhangani & Van Wyk, 2013). The HRS ability of Maillard-
type conjugates is probably due to the chelating activity of the com-
pounds against the metal ions that participated with H2O2 to form HRs
(Han et al., 2017), which, in turn, can prolong the Fenton reaction (Nie,
Zhao, Regenstein, Xu, & Meng, 2017). Studying antioxidant activity of
MRPs between glucose-glycine, Yoshimura, Iijima, Watanabe, and
Nakazawa (1997) declared that HMW fractions (> 14 kDa) of MRPs
showed more HRS activity than LMW ones (< 14 kDa). Although, the
obtained MRPs at the initial heating time (1.0 h) showed the highest
HRS activity, due to their suppressive effect by chelating Fe2+, pro-
longed Maillard reaction resulted in MRPs with strong reducing activity
which were able to reduce Fe3+ obtained from Fenton reaction to Fe2+
(promotive effect). It is worth noting that the Maillard reaction can
generate H2O2 through degrading Amadori products (via 1,2- and 2,3-
enolization routes), oxidizing enolate anion, and autooxidizing the
saccharide moiety, which can subsequently react with metal ions to
generate HR (Perusko et al., 2015). This indicates that MRPs can react
with free oxygen molecules to form H2O2. In this way, MRPs can be
M. Nooshkam et al.
easily oxidized and sacrificed in the presence of oxygen compared to
lipids, leading to oxygen unavailability to involve the oxidation reac-
tion.
4.1.6. Chelating activity on ferrous ion
There are documented reports that transition metals, especially iron
and copper, are necessary for producing free radicals through Fenton
reactions. As well, they can initiate and propagate the lipid peroxida-
tion. Among different species of metal ions, Fe2+ ion has the highest
pro-oxidant effect and, therefore, compounds with metal chelation ac-
tivity play a key role in the concentration decrement of the transition
metals that are implicated in lipid peroxidation (Bai, et al., 2017). The
ion-chelating affinity of MRPs has been reported and hydroxyl or pyr-
role groups are attributed to their antioxidant activities (Morales,
Fernández-Fraguas, & Jiménez-Pérez, 2005; Gu et al., 2010). HMW
MRPs (> 50 kDa) obtained at the final stage of the Maillard reaction
showed higher metal-chelating activity than LMW ones (Gu et al.,
2010). Metal chelating activity of MRPs is partially due to the anionic
nature of melanoidins, which makes them chelators of transition me-
tals, and nitrogen atom in their structure can chelate copper ion. It was
proposed that hydroxyl and/ or ketone groups of pyridone or pyranone
compounds may function as chelation donors in melanoidins (Fig. 2A)
(Morales et al., 2005; Wang et al., 2011). Moreover, the chelating
properties of thiol groups in thiol-derived MRPs and hydroxyl groups of
Amadori products have been reported by Sproston and Akoh (2016).
Kim and Lee (2009) proved that MRPs obtained from glucose-glycine/
diglycine/triglycine had higher binding (chelating) ability to iron than
copper, which was congruent with the findings of Ruiz-Roca, Navarro,
and Seiquer (2008), working on metal chelating behavior of glucose/
lysine heated mixtures. It was also revealed that MRPs CML and Nε-
fructoselysine can form moderately stable complexes with copper, but
they did not form complexes with zinc (Seifert, Krause, Gloe, & Henle,
2004).
4.1.7. Superoxide anion (O2−) scavenging (SAS) activity
The superoxide radicals are produced through many biological re-
actions and indirectly initiated lipid oxidation. Highly reactive HR and
singlet oxygen are formed from superoxide radical anions (O2−) and
H2O2, which contribute to lipid peroxidation in biological systems. SAS
activity is therefore used for indirect evaluating of antioxidant activity.
The ability of MRPs to scavenge O2− has been reported in previous
researches (Chawla, Chander, & Sharma, 2009; Rao et al., 2011) and
SAS activity increased as a function of heating time (Yen & Hsieh, 1995;
Yoshimura et al., 1997). Yoshimura et al. (1997) showed that MRPs
render strong reducing power and act as direct inhibitors for O2−. The
authors also noted that the autooxidation of sugars during the Maillard
reaction resulted in O2− generation, which might be a reason for lower
rate of SAS activity than HRS. MRPs inhibition towards O2− has been
ascribed to the brownish pigments of Maillard glycation (Yen & Hsieh,
1995).
4.1.8. Antioxidant activity in sodium dodecyl sulfate (SDS)/linoleic acid-
AAPH system
In this assay, the radical reaction is started by adding AAPH (2,2′-
azobis(2-amidinopropane) dihydrochloride) to the SDS micelle-linoleic
acid peroxidation system (containing phosphate buffer, SDS, and lino-
leic acid). The effect of MRPs on oxidation of linoleic acid in the ob-
tained SDS/linoleic acid-AAPH system is measured spectro-
photometrically at 234 nm and then expressed as inhibitory activity (%)
towards the formation of conjugated dienes (Sun, Hayakawa,
Chuamanochan, et al., 2006). Sun, Hayakawa, Chuamanochan, et al.
(2006) reported that lipid oxidation rates significantly slowed down in
the presence of glycated ovalbumin (OVA) with different D-aldo-
hexoses. This may be attributed to the presence of reductones and
aminoreductone structures in MRPs, especially HMW ones (> 3.5 kDa)
for which the reducing and metal chelating properties have been noted
649
Food Chemistry 275 (2019) 644–660
for the antioxidant mechanism of MRPs (Kitts & Hu, 2005). As well, it
was shown that melanoidins with higher Abs 420 nm exerted greater
inhibitory effect against AAPH-triggered linoleate oxidation in an
aqueous dispersion, which was ascribed to the chromophores with PRS
property attached to the melanoidin skeleton (Morales & Jiménez-
Pérez, 2004).
4.1.9. β-Carotene bleaching assay
A hydrogen atom abstraction from the diallylic methylene group of
linoleic acid leads to the formation of free radicals, which in turn attack
the β-carotene molecule following rapid discoloration. The rate of β-
carotene bleaching is decreased in the presence of antioxidants, which
neutralize the generated free radicals during incubation at 50 °C. The
mechanism of β-carotene bleaching consists of a free radical-mediated
phenomenon triggered by hydroperoxide formation from linoleic acid
(Rao et al., 2011). The inhibiting activity of radiation-derived MRPs on
bleaching of β-carotene has been reported in lysine/glycine-glucose
(Chawla, Chander, & Sharma, 2007) and chitosan-glucose (Rao et al.,
2011) systems. In another study, MRPs between ultrasound-treated
smooth hound viscera proteins and sucrose exhibited more β-carotene
bleaching protection effect than those obtained via conventional
heating, due to physicochemical and structural changes induced by
ultrasound pretreatment (Abdelhedi et al., 2017).
4.1.10. Oxygen radical absorbing capacity (ORAC)
The ORAC assay has been extensively used as a standard method to
determine antioxidant activity of diverse compounds (Su et al., 2011).
In this assay, MRPs can scavenge PRs generated by AAPH and therefore
inhibit lipid oxidation in model and food systems (Yilmaz & Toledo,
2005). Kitts and Hu (2005) reported that the determination of total
antioxidant activity of MRPs using the ORAC assay yielded an excellent
basis for evaluating the ability of MRPs to scavenge oxygen radicals
between various sugar reactant sources. They also showed that ORAC
results of MRPs obtained by heating the solution containing different
sugars (glucose, fructose, and ribose) and lysine were in line with the
DPPH measurements. Su et al. (2011) stated that glycation reaction of
peanut hydrolysate led to the creation of volatile compounds and
melanoidins with notably higher ORAC compared to unconjugated
counterpart.
4.1.11. Assay of tetrazolium salt XTT reducibility
This assay is used to monitor the extent of the Maillard reaction
based on the reduction of XTT (2,3-bis(2-methoxy-4-nitro-5-sulfo-
phenyl)-2H-tetrazolium-5-carboxanilide) to a water-soluble formazan,
which can be used for photometric assay (Sun et al., 2004). Sugar–-
protein complexes from the Maillard reaction act as potent antioxidants
and exhibit reducing activity against XTT (Sun et al., 2004; Sun,
Hayakawa, Chuamanochan, et al., 2006; Sun, Hayakawa, Puangmanee,
et al., 2006). XTT reducibility showed a linear relationship with con-
centration of glycated egg white. As well, strong correlations were
observed between XTT reducibility and browning index (0.905) and
fluorescence intensity (0.978), indicating that the formation of sub-
stances with XTT-reducing behavior was closely related to the pro-
gression of browning color and fluorescence intensity of MRPs (Sun
et al., 2004).
Other available methods like determination of peroxide value,
thiobarbituric acid reactive substances (TBARS), p-anisidine, and oxi-
dative stability using the Rancimat have been successfully used for
evaluating the antioxidant activity of MRPs (Vhangani & Van Wyk,
2016).
4.2. Antioxidant activity of MRPs in model systems and factors influencing
their functionality
There are many studies concerning the antioxidant activity of MRPs
in model systems (Table 2). The Maillard reaction can be performed
M. Nooshkam et al.
Fig. 2. Different mechanisms proposed for antioxidant effect of the Maillard reaction products (MRPs): (A) Metal chelation of pyranone and hydroxypyridone of
melanoidins (designed with respect to Bailey and Um, 1992) and (B) free radical chains termination.
through dry and wet heating procedures. The dry method has some
advantages like the requirement of less space and time, higher shelf-life,
feasible handling and storage of the final product, more reproducibility,
and lower negative effects on the protein structure. In addition, it has
some limitations, such as the need for solid reactants and controlled
relative humidity (RH), which make it inappropriate for industrial scale
than the wet heating method. Conversely, the heating in solution (wet
heating) can be easily performed in solution under prevailing condi-
tions, like pH, temperature, time, and in the presence of reducing sugars
and amino-bearing compounds (Karbasi & Madadlou, 2018). According
to Table 2, the Maillard reaction improves the antioxidant ability of
proteins, peptides, and amino acids, and the extent of antioxidant ac-
tivity depends on the Maillard reaction conditions such as pH, time,
temperature, RH, and reactant type/concentration, which are discussed
hereunder.
4.2.1. Temperature and reaction time
Temperature and reaction time are the most important and inter-
dependent factors that influence the glycation degree of the Maillard
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Food Chemistry 275 (2019) 644–660
reaction in both dry and wet heating methods. It is generally agreed
that the rate of non-enzymatic reaction is slow at 35 °C and increases at
temperatures over 55 °C and most studies dealing with the Maillard
reaction have been usually carried out at temperatures between 55 °C
and 120 °C. The range of reaction time can vary from 30 min to 24 h and
also up to several days (Lee et al., 2017). Proteins undergo denaturation
at high temperatures usually employed in the Maillard reaction, which
can unmask some amino acid residues with electron-donating potential
(Hamdani et al., 2018). Rising reaction temperature and time often lead
to higher glycation yield and browning intensity, due to the fact that
more denatured proteins are now available to contribute to the Maillard
reaction. Based on the Arrhenius theory, increasing temperature leads
to an increase in molecules’ kinetic energy, collision frequency, and the
Maillard conjugates formation rate (Lee et al., 2017). Nasrollahzadeh
et al. (2017) found that microwave conjugates had higher DPPH-RS
ability than those obtained by conventional heating, probably due to
the increased Maillard reaction rate under microwave, which resulted
in an increase in content of advanced products with superb anti-
oxidative activity. Moreover, a good correlation was observed between
 Table 2
Summary of some studies dealing with the antioxidant activity of Maillard reaction products (MRPs).
System Maillard reaction conditions Antioxidant assay Observations References

pH Time (h) Temp (°C) Protein: RH (%) Heating

M. Nooshkam et al.

sugar ratio method

In vitro
Lysine/xylose 9 1–5 100 2:1 Wet Reducing power Antioxidant activity increased as a function of heating time, except for reducing power and Yen and Hsieh (1995)
DPPH-RS activity DPPH-RS activity, which the former had decreasing trend likely due to the decomposition
Superoxide anion of reducing components during prolonged heating and the latter showed ∼50% scavenging
scavenging activity but non-significant trend during heating period.
activity
HRS-activity
Peroxide
inhibition
β-LG/arabinose, galactose, 6.5 72 60 1:1 Wet DPPH-RS activity β-LG/ribose and β-LG/arabinose conjugates showed the highest DPPH-RS activities (∼80 Chevalier et al.
glucose, lactose, and 60%, respectively). Protein-lactose MRPs had the lowest antioxidative activity. (2001)
rhamnose, and ribose
PPP/glucose, fructose and 7.6 5 100 2:1 and Wet DPPH-RS activity The conjugation reaction enhanced the antioxidant activity as a function of heating time. Benjakul et al. (2005)
galactose 1:1 Reducing power
Lysine/glucose, fructose and 9 1 121 1:1 Wet DPPH-RS activity MRPs exhibited higher antioxidant activities than unreacted mixture. Kitts and Hu (2005)
ribose ORAC
Ovalbumin/allose, altrose, 48 55 12.5:1 65 Dry Tetrazolium salt All conjugates showed greater antioxidative ability than heated control and unheated Sun, Hayakawa,
talose, galactose, XTT reducibility ovalbumin and antioxidant capacity was in line with browning intensity. Chuamanochan, et al.
mannose, gulose, and DPPH-RS activity (2006)
glucose ABTS-RS activity
Antioxidant
activity in SDS/

651
linoleic acid-
AAPH system
α-LA/allose 48 50 1:13 55 Dry Tetrazolium salt α-LA glycated with allose had the highest antioxidant activity. Sun, Hayakawa,
XTT reducibility Puangmanee, et al.
ABTS-RS activity (2006)
PPP/glucose 8–12 8 100 1:1 Wet DPPH-RS activity The MRPs obtained at higher pH values showed higher antioxidant activities. Lertittikul et al.
Reducing power (2007)
Glycine, diglycine, and 7.8 4 100 1:1 Wet FRAP The DPPH-RS and ABTS-RS activities and FRAP of all MRPs increased as a function of Kim and Lee (2009)
triglycine/glucose Cu2+ and Fe2+ heating time.
chelating The cupric and ferrous ion chelating abilities of all MRP samples increased and then
activities decreased as a function of heating time, but the latter was much higher than the former.
DPPH-RS activity
ABTS-RS activity
Casein/glucose 12 2.16 102 1:2 Wet DPPH-RS activity Antioxidant activities of MRPs with different molecular weights were distinctly different. Gu et al. (2009); Gu
Reducing power et al. (2010)
Chelating activity
on ferrous ion
a
Chitosan/glucose 1:1 Wet DPPH-RS activity MRPs with significant antioxidant activity were produced after irradiation. Rao et al. (2011)
Reducing power
Superoxide anion
scavenging
activity
β-carotene
bleaching assay
α-LA and β-LG/ribose 8.4 5 95 1:1 Wet DPPH-RS activity α-LA/ribose and β-LG/ribose MRPs showed boosted antioxidant activities. Jiang and Brodkorb
Reducing power (2012)
Bioactive tripeptide IPP (Ile- 9 8 98 1:2 Wet DPPH-RS activity Reducing power and DPPH-RS activity of IPP–ribose MRPs increased significantly with Jiang et al. (2013)
Pro-Pro)/ribose Reducing power heating time.
(continued on next page)
Food Chemistry 275 (2019) 644–660
 Table 2 (continued)

System Maillard reaction conditions Antioxidant assay Observations References

pH Time (h) Temp (°C) Protein: RH (%) Heating

M. Nooshkam et al.

sugar ratio method

Lysine/fructose and ribose 9 0.25–2 60–121 1:1 Wet DPPH-RS activity The antioxidant activity (except for HRS activity) of fructose/lysine increased as a function Vhangani and Van
Reducing power of reaction temperature, while the reaction progress lowered the antioxidant capacity of Wyk (2013)
HRS-activity ribose/lysine systems.
PRS- activity
b
Whey proteins/arabinose 8 1 1:3 Wet DPPH-RS activity Ultrasound-induced Maillard reaction generated the conjugates with significant Perusko et al. (2015)
Reducing power antioxidative activity.
Inhibition of lipid
peroxidation
Lysine and glycine/ribose and 4 and 9 0.5–2.16 60–121 1:1 Wet PRS-activity PRS-activity and reducing power enhanced significantly as a function of temperature and Vhangani and Van
fructose DPPH-RS activity time (fructose-lysine < fructose-glycine < ribose-lysine < ribose-glycine). Wyk (2016)
Reducing power MRPs obtained at 121 °C had higher DPPH-RS activity than BHA.
Whey protein isolate (WPI) 6 0.75 90 1:1 Wet DPPH-RS activity The Maillard reaction generated conjugates with boosted antioxidant potency than Nooshkam and
and whey protein unreacted mixtures. Madadlou (2016a)
hydrolysate (WPH)
/lactose and purified
lactulose
Chicken peptide/glucose 0.5–4 90–150 1:1 to 1:5 Wet DPPH-RS activity MRPs showed reducing power and DPPH-RS activity, while HRS activity and chelating Bai et al. (2017)
Reducing power activity on ferrous ion were not influenced after glycation.
HRS-activity
Chelating activity
on ferrous ion
c
Chicken bone hydrolysate/ 7.5 100 2.4 Wet DPPH-RS activity Antioxidant ability of MRPs increased as a function of heating time. Nie et al. (2017)
galactose Reducing power

652
HRS-activity
Bovine serum albumin (BSA)/ 7.85 0.25–2 90 1:1, 1:3 Wet DPPH-RS activity Microwave radiation formed conjugates with boosted antioxidative capacity than those Nasrollahzadeh et al.
maltodextrin and 1:5 obtained from convectional heating due to higher reaction rate of Maillard reaction under (2017)
microwave heating.
Lysozyme/Guar gum 240 60 1:1 80 Dry DPPH-RS activity Conjugated lysozyme had significantly higher antioxidant activity than unconjugated (Hamdani et al.,
Reducing power counterpart. 2018)

In vivo
Brown diet rich in MRPs Although, brown diet showed strong in vitro antioxidative property; however, oxidative Seiquer et al. (2008)
(chocolate, breakfast damage markers (i.e. erythrocyte hydroperoxides and serum TBA substances) and
cereal, baked products, antioxidative defense parameters such as serum antioxidants and the activity of enzymes
and fried, toasted, and including glutathione peroxidase, superoxide dismutase, and catalase remained unchanged
breaded foods) and white in healthy male adolescents after consumption of two diets for 2 weeks.
diet poor in MRPs However, MRPs-rich diets revealed a protective role towards triggered oxidation.
Chocolate, coffee (raw and Oxidative resistance of human low-density lipoprotein (LDL) was studied in blood plasma Dittrich et al. (2009)
roasted), pretzel sticks, of healthy volunteers after consuming foods rich and poor in MRPs for 3 weeks. The
beer (pale and dark), milk consumption of heat treated foods (rich in MRPs) led to a 35.5% increase in oxidant
(fresh and condensed), resistance of LDL in comparison to those poor in MRPs.
and bread (crust and
crumb)
Half-fin anchovy hydrolysates 9 1.66 120 Wet The administration of MRPs increased glutathione peroxidase and superoxide dismutase Song, Shi, Yang and
(HAHp)-glucose activities and reduced lipid peroxidation in mice, particularly in the liver. Wei (2018)

a
Aqueous mixture irradiated for up to 100 kGy.
b
Mixture sonicated at 20 kHz frequency and output power of 9.5 W (135 W/cm2).
c
Final concentration.
Food Chemistry 275 (2019) 644–660
M. Nooshkam et al.
antioxidant effect and browning intensity, owing to the formation of
melanoidins with documented antioxidant properties. Increased anti-
oxidant property (based on reducing power, DPPH-RS, and PRS activ-
ities) of fructose-lysine MRPs as a function of heating time and tem-
perature has also been reported by Vhangani and Van Wyk (2013).
Bai et al. (2017) demonstrated that DPPH-RS and reducing power of
chicken peptide-glucose MRPs increased significantly as the reaction
temperature rose from 90 to 110 °C and then no significant differences
were observed up to 150 °C. The authors stated that melanoidins, re-
ductones, and also some heterocyclic components formed at high
temperatures are responsible for the increased antioxidant activity of
MRPs obtained by heating chicken peptide with glucose. A positive
correlation (R2 ≥ 0.93) was found between rising temperature
(37–60 °C) and time with antioxidant effect of MRPs synthesized from
WPI and lactose; the slope of DPPH-RS activity was significantly in-
creased one order as the temperature rose about 10 °C. As well, the
antioxidant capacity increased as the percentage of reactive lysine de-
creased (Yáñez, Gagneten, Leiva, & Malec, 2018).
It can be concluded that high temperatures and longer periods of
reaction time usually result in more glycation degree concomitant with
greater levels of intermediate and brownish MRPs with high molecular
mass. In this regard, more electron and hydrogen donors (e.g., hydroxyl
and pyrrole groups) are formed in conjugation with melanoidins with
metal sequestrating effect (due to anionic nature), thereby strength-
ening the antioxidative potential of MRPs. It is worth mentioning that
intense temperatures may also lead to MRPs degradation or complexity
and limit their antioxidation.
4.2.2. Reactant type and concentration
The glycation degree and subsequently the antioxidant capacity of
Maillard-type conjugates can be influenced by the type of reactants
(protein or carbohydrate) and their molar ratios. The reactivity of LMW
compounds is greater than HMW ones, due likely to the higher steric
hindrance of the latter. Consequently, aldopentoses possess more re-
activity than aldohexoses and monosaccharides exhibit greater re-
activity than di- or oligosaccharides (Rufián-Henares, García-Villanova,
& Guerra-Hernández, 2004). As well, aldose sugars have higher re-
activity than ketose sugars because the carbonyl group of the latter is
sterically more hindered than the former (O’Brien et al., 1989). MRPs
obtained from protein-sugar model systems rendered lower anti-
oxidative activity than those prepared from amino acid-sugar model
systems (Lingnert & Eriksson, 1980). It was found that molecular
weight distribution of peptides could influence their antioxidant prop-
erties; peptides with smaller molecular weight would possess higher
reaction degrees and cross-link easily with sugars in the Maillard re-
action, which can subsequently form volatile components with superior
antioxidant effect (Yu et al., 2018).
A study conducted by Sun, Hayakawa, Chuamanochan, et al. (2006)
demonstrated that the ABTS-RS and DPPH-RS activities of MRPs ob-
tained from OVA and different D-aldohexoses (allose, altrose, talose,
galactose, mannose, gulose, and glucose) were correlated well with the
browning intensities, and antioxidant capacity of the complexes were as
following order: altrose/allose-OVA > talose/galactose-OVA >
gulose-OVA > mannose/glucose-OVA. Sugar epimers about C-2 had a
similar antioxidative activity and the authors reported that the ad-
vanced crosslinking reaction was not influenced by the configuration of
the hydroxyl group about position C-2, whilst the formation of MRPs
and subsequently their antioxidative capacities were markedly influ-
enced by the configuration of OH groups about C-3 and C-4. In another
study, six different sugars, ribose, arabinose, rhamnose, glucose, ga-
lactose, and lactose, were glycated with β-LG (Chevalier, Chobert,
Genot, & Haertlé, 2001). β-LG-ribose and β-LG-lactose conjugates had
the highest and lowest DPPH-RS activities, respectively (∼80% vs.
∼10%). Sugars arabinose, rhamnose, glucose, and galactose showed
about 60, 35, 24, and 20% DPPH-RS activity when glycated with β-LG,
respectively.
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Food Chemistry 275 (2019) 644–660
Benjakul, Lertittikul, and Bauer (2005) stated that galactose-porcine
plasma protein (PPP) MRPs had higher reducing power and DPPH-RS
activity than those obtained from glucose and fructose. Although, as
previously mentioned, the reactivity of aldose sugars is higher than that
of ketose sugars, the authors reported that MRPs from glucose had the
lowest antioxidant capacity compared to galactose and fructose-protein
MRPs. Furthermore, Hwang, Kim, Woo, Lee, and Jeong (2011) found
that MRPs obtained from amino acids-fructose model systems exhibited
higher DPPH-RS, ABTS-RS, and angiotensin converting enzyme (ACE)-
inhibitory activities than those obtained from amino acids-glucose
model systems. These controversial results could be ascribed, in some
cases, to an indirect relationship between reactant reactivity and anti-
oxidant activity (Sun, Hayakawa, Puangmanee, et al., 2006).
The excess of reducing sugars to amino groups-bearing compounds
accelerates the rate of Maillard reaction, probably due to mechanistic
differences between destruction of sugars compared to amino acids
(O’Brien et al., 1989). Dong, Wei, Chen, McClements, and Decker
(2011) stated that the antioxidant activity of MRPs obtained from
casein peptide-glucose was significantly influenced by the glucose
concentration and peptide:glucose ratio of 1:2 had the highest DPPH-RS
activity than the other ratios 1:0.5 and 1:1. Glycation degree, Abs
294 nm, and Abs 420 nm (browning intensity) increased significantly as
a function of peptide:glucose ratio and heating time, suggesting that
more advanced Maillard products with antioxidative properties were
formed. Likewise, MRPs containing higher concentration of reducing
sugars glucose, galactose, and fructose had more reducing power than
those obtained from low levels of sugars and the antioxidant activity
was in line with the results of Abs 294 nm and browning intensity
(Benjakul et al., 2005). Also, the reducing power of chicken peptide-
glucose MRPs was significantly increased as the ratio of glucose:peptide
rose from 1:1 to 3:1 and then declined remarkably at higher ratios of
glucose to peptide. The highest DPPH-RS capacity (77.80%) was ob-
tained when glucose to peptide ratio increased to 4:1 and then de-
creased slightly at 5:1 ratio (Bai et al., 2017). The decreased antioxidant
property at high levels of sugars could be due to high glycation degree
and rapid Maillard progression, leading to MRPs complexity with lower
antioxidant effect. Similar explanations were given by Vhangani and
Van Wyk (2013), working on RS activity of ribose-lysine MRPs.
Despite the fact that high sugar concentration compared to amino
groups increases the glycation yield and forms HMW conjugates, it
usually increases the solution viscosity and subsequently limits further
early MRPs transformation to products with antioxidant property. This
is evident in systems containing proteins and polysaccharides, in which
the system viscosity can be significantly increased after the Maillard
conjugation and sometimes gel-like structures may be observed, due to
pH reduction during the Maillard reaction, allowing the isoelectric
point of the protein to be reached. Therefore, viscosity increment limits
the molecule mobility and the reaction progression to the final stage,
lowering the formation of antioxidant compounds.
4.2.3. pH
The initial pH value of the aqueous solution containing reducing
sugars and amino compounds influence the rate and direction of the
Maillard reaction. Generally, most of the studies concerning the
Maillard reaction were performed at alkaline conditions (pH > 7.0),
because the solubility of proteins is higher at basic pH values and
consequently more soluble protein is available to react with reducing
sugars during the non-enzymatic glycation reaction (Lee et al., 2017).
Acidic pH values provide a low reaction rate due to eNH3 groups
protonation and an increasing trend in the rate is observed afterwards
with rising pH value up to ∼10. Further increase in pH leads to a de-
crease in the browning rate, likely due to the lack of sufficient H+ ions
to catalyze Amadori and Heyns rearrangements. It is worth noting that
ARPs degradation pathways also depend on the pH value (1,2- and 2,3-
enolization routes at low and alkaline pHs, respectively) (O’Brien et al.,
1989).
M. Nooshkam et al.
Lertittikul et al. (2007) found that PPP–glucose MRPs obtained at
high initial pHs presented greater reducing power and DPPH-RS ac-
tivity, due to higher contents of intermediate and final products at such
pH values, since these compounds exhibit superb antioxidant proper-
ties. Similarly, the reducing power and DPPH-RS activity of MRPs ob-
tained by glycation of WPI with xylose, glucose, fructose, lactose, and
maltose were improved with increasing pH values from 3.0 to 9.0
(Wang et al., 2013). Antioxidant ability was correlated well with the
browning intensity and this may explain why MRPs with high browning
intensity possess good antioxidant activity. In another study, the anti-
oxidant activity of half-fin anchovy hydrolysates (HAHp) -glucose
Maillard-type conjugates was evaluated by Song, Yang, Wei, and Ruan
(2016). The higher pH value resulted in a conjugate with greater re-
ducing power, while the DPPH-RS activity of conjugates declined with
increasing pH values to alkaline conditions and MRPs obtained at initial
pH of 5.6 showed higher DPPH-RS capacity than those obtained at pH
value of 9.6 (95.30% vs. 39.57%). The authors hypothesized that the
improved reducing power at high initial pHs could be related to the
HMW compounds produced during the Maillard reaction, while the
relatively LMW compounds obtained at low pHs might be responsible
for the increased DPPH-RS activity of the MRPs. From our point of
view, the increased DPPH-RS effect at lower pH values is due to the fact
that such pH values result in lower glycation rate and mainly control
the Maillard reaction to form early MRPs. It was reported in some
studies that DPPH-RS activity is usually found in the early stages of the
Maillard reaction (Liu et al., 2014).
4.2.4. Water activity (aw)/RH
The adjustment of aw/RH is a critical step in the dry-heating method
of the Maillard reaction. In dry-heating mode, the reaction is usually
performed over a temperature range of 40 to 80 °C, where 60 °C is the
most commonly used temperature. Furthermore, RH is mainly con-
trolled at 65% or 79% moisture by means of saturated potassium iodide
or potassium bromide, respectively (de Oliveira et al., 2016). The op-
timal rate of glycation reaction observed at intermediate aw values and
RH increment from 50 to 80% (aw = 0.5–0.8) increased the glycation
degree of Maillard reaction (Martinez-Alvarenga et al., 2014). The re-
action rate is decreased and fairly self-inhibited at higher RHs due to
lower reactant concentration, derived from water rescue during some
stages (Karbasi & Madadlou, 2018). Wijewickreme, Kitts, and Durance
(1997) found that glucose-lysine MRPs obtained at initial reaction
conditions, i.e., 74 and 78% RHs, showed greater metal-chelating affi-
nity than those obtained at other RHs (57–95%). Also, initial RHs 62%
and 68% led to the formation of fructose-lysine MRPs with higher
copper chelating activity than other initial RHs. These findings suggest
that intermediate aw values play an important role in the formation of
MRPs with high glycation degrees, which in turn lead to a Maillard-
based conjugate having boosted antioxidant activity.
4.3. Antioxidative activity in actual food systems
4.3.1. Bakery products
The Maillard reaction occurs under high temperatures applied in
baking processes. The reaction leads to formation of MRPs in the bread
crust which are essential to improve the flavor, color, and texture of the
final product (Michalska, Amigo-Benavent, Zielinski, & Del Castillo,
2008). Michalska et al. (2008) evaluated the effect of bread making on
the formation of MRPs contributing to the overall antioxidant activity
of rye bread. Their results showed that the baking process led to the
formation of MRPs (mainly melanoidins) in the obtained rye bread,
which were able to scavenge the peroxyl and ABTS radicals and reduce
Folin-Ciocalteu reagent. They also reported that the water content de-
creased quickly on the dough surface, leading to favorable conditions
for the formation of higher MRPs and colors in the crust.
Lipid oxidation is the main problem in fat-containing and dry foods
such as cookies, which results in rancidity and thus decreases the shelf
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Food Chemistry 275 (2019) 644–660
life and storage stability of the product (Lingnert, 1980; Bressa, Tesson,
Dalla Rosa, Sensidoni, & Tubaro, 1996). MRPs obtained from heated
solutions and real food products containing reducing sugars and amino
acids have been used to decrease the lipid oxidation rate in model and
food systems (Vhangani & Van Wyk, 2016; Michalska et al., 2008). The
Maillard browning reaction could reduce the availability of oxygen (as
a reactant for peroxidative reactions) and metal catalysts; the latter can
initiate peroxidative chain reactions by decomposing lipid hydroper-
oxides. In this regard, the rate of lipid oxidation was markedly de-
creased in the presence of MRPs, mainly due to the inhibitory effect of
MRPs on the formation of aldehydic lipid oxidation products as markers
of the extent of oxidation reaction (Bressa, et al., 1996). Lingnert
(1980) studied the effect of formed MRPs (from histidine and glucose)
during baking on the storage stability of two basic types of cookies
(containing lard and vegetable fat) stored at 30 °C. In cookies con-
taining lard (the least stable cookie), rancid flavor development and n-
hexanal formation were markedly retarded in the presence of histidine
and glucose. The cookies containing vegetable fat showed similar re-
sults, but the effect was less pronounced. They argued that the anti-
oxidative effect is mainly due to the formation of MRPs from histidine
and glucose during the baking process.
The chain-breaking antioxidant capacities of the MRPs have also
been reported in butter cookies (Bressa et al., 1996). MRPs produced
during the first 20–30 min of cooking showed a high antioxidant ca-
pacity (up to 5.0 g of Trolox in 100 g of dried aqueous extracts of the
cookies), indicating the essential effect of MRPs on the oxidative sta-
bility and shelf life of processed foods. González-Mateo, González-
SanJosé, and Muñiz (2009) isolated LMW (< 3 kDa) and HMW
(> 3 kDa) MRPs from commercial muffins and reported that the latter
had higher antioxidant activity. The potent antioxidant properties of
MRPs isolated from biscuit (Martín et al., 2009; Patrignani, Rinaldi, &
Lupano, 2016) and cookies (Sun, Hayakawa, Ogawa, Fukada, &
Izumori, 2008) have also been reported. These studies suggest that
MRPs besides their critical roles in color and flavor of bakery products,
possess appreciable antioxidant activity, and act as preservative agents
in these products. In addition, the Maillard conjugates have mainly
higher thermal stability than their individual precursors
(Nasrollahzadeh et al., 2017; Perusko et al., 2015) and, therefore, they
can be used in thermally processed foods as antioxidants and emulsi-
fiers without there being remarkable degradation and losing their
techno-functional and biological attributes under employed tempera-
tures.
4.3.2. Pasta products
The antioxidant and anti-mutagenic properties of both intermediate
and final Maillard reaction products (melanoidins) are well docu-
mented (Anese, Nicoli, Massini, & Lerici, 1999). Therefore, Zhu et al.
(2013) used MRPs prepared from chitosan and xylose and evaluated
their effects on the preservation and quality of semi-dried noodles. The
product containing 0.25–0.35% MRPs had significantly higher
springiness, hardness, maximum shear force, breaking distance, and
lower cooking loss mainly due to the good surface activity of MRPs,
which are able to interact with gluten and starch molecules, yielding a
gluten network with more compact structure. In addition, MRPs at in-
corporation level of 0.35% (6.0 h heating) increased the shelf life of the
semi-dried noodles for more than 7.0 days compared to the control
noodles stored at ambient temperature. The noodles had significantly
less dark in color in the presence of MRPs, which was attributed to the
MRPs inhibitory effect on PPO. The antioxidant potential of MRPs
produced in pasta during drying was also reported by Anese et al.
(1999).
4.3.3. Potato products
Fried potato products such as French fries and crisps are extensively
consumed all over the world. The Maillard reaction plays an important
role in the development of color and also flavor of these products.
M. Nooshkam et al.
Serpen and Gökmen (2009) evaluated the antioxidant capacity of po-
tato crisps as a result of the Maillard reaction. Potato crisps had high
antioxidant ability, mainly due to the formation of melanoidins during
frying, which in turn may lead to an increase in shelf-life through re-
tarding the oxidation process. They argued that besides the antioxidant
activity derived from melanoidins, potato crisps have negative impacts
on health due to the formation of acrylamide during frying.
4.3.4. Meat products
In meat and meat products, the quality deterioration is due to lipid
oxidation, which can directly influence the main properties, such as
texture, flavor, color, and nutritive value. It has been reported that
cooked meat has more susceptibility towards lipid oxidation reaction
compared to uncooked meat, mainly due to the oxidation of its highly
unsaturated membrane phospholipids. Meat grinding disrupts its
muscle cell membranes, leading to phospholipid exposure to high
oxygen and light. Moreover, the heating process denatures meat pro-
teins and increases the release rate of non-heme iron and poly-
unsaturated fatty acids (PUFA) from meat. In addition, oxidative ran-
cidity development in cooked meat products is a major issue in
marketplaces, restaurants, and fast foods for airline industries (Alfawaz,
Smith, & Jeon, 1994). Thus, the use of food grade antioxidants is
needed to decrease or inhibit the lipid oxidation reaction and MRPs are
one of the natural antioxidants that can be used for this purpose.
In a study, the antioxidant activity of MRPs (autoclaving the mix-
ture of glucose and egg albumin/or soy protein isolate hydrolysates)
was investigated in cooked ground beef based on the TBA values and
headspace gas chromatographic analysis during 8.0 days of storage
period at 4.0 °C. Results revealed that incorporation level of 1.0% MRPs
(1.0 h heating) completely inhibited the development of rancid flavor,
according to the TBA values and hexanal and pentanal levels (Alfawaz
et al., 1994). The rancidity retardation in frozen pork sausage in the
presence of MRPs from glucose and histidine was also reported by
Lingnert and Lundgren (1980). In another study, MRPs (obtained from
the mixtures of reducing sugars glucose, xylose, and dihydroxyacetone
and free amino acids arginine, histidine, leucine, lysine, and trypto-
phan) were incorporated (3.0% v/w basis) into fresh ground pork pat-
ties (Bedinghaus & Ockerman, 1995). The patties were cooked (internal
temperature of 68 °C) and evaluated for TBA value over 10 days of
storage at 4.0 °C. MRPs showed significant inhibition against lipid
oxidation in ground pork patties. Recently, Fernández, Fogar, Doval,
Romero, and Judis (2016) evaluated the antioxidant effect of bovine
plasma proteins modified via the Maillard reaction on n-3 fortified beef
patties. The MRPs at level of 3.0% showed a marked inhibition effect on
both stages of lipid oxidation; inhibition percentage of peroxidation
was > 70% on hydroperoxides formation and > 45% on TBARS.
PUFA in foods, especially fish products are susceptible to auto-
xidation leading to the development of rancid flavor and shelf life de-
crement of many food products. Tanaka, Kuei, Nagashima, and Taguchi
(1988) obtained MRPs by refluxing a mixture of L-histidine and D-
glucose at pH 5.0, 7.0, and 9.0 for up to 24 h. The antioxidative activity
of MRPs increased as a function of reaction time (especially at the later
stage of the Maillard reaction), reducing power development, and
higher initial pH value. They also used 0–5.0% MRPs (initial pH 9.0 and
24 h heating time) in Kamaboko-type sardine products (boiled or deep-
fried sardine minced meats) and the autoxidation reaction in the pre-
sence of MRPs was effectively inhibited in the sardine products stored
at 4.0 °C. The oxidation of ground chicken breast was successfully
lowered in the presence of 0.1 or 0.2 mg g−1 MRPs from heating glu-
cose-arginine, valine, or histidine solutions (Miranda, Rakovski, &
Were, 2012). Refrigerated fresh pork meat incorporated with xylan–-
chitosan MRPs (heated for 60 and 120 min) showed lower lipid oxi-
dation (Li, Shi, Jin, Ding, & Du, 2013). Antony, Han, Rieck, and Dawson
(2002) incorporated turkey meat with dry honey or preformed honey-
lysine MRPs and argued that heating of turkey meats containing dry
honey led to the formation of MRPs with better dispersibility/solubility
655
Food Chemistry 275 (2019) 644–660
and antioxidative activity than those loaded with preformed MRPs. In
another study, ground roasted coffee was used as rosemary replacement
in raw ground top round beef and the oxidation of the product was
significantly decreased in the presence of NaCl (as a prooxidant of lipid
oxidation) mainly due to MRPs presented in roasted coffee (Lin, Toto, &
Were, 2015). It has been reported that sodium chloride exerted a con-
centration-dependent prooxidant effect in meats through (i) disrupting
cell membranes and subsequently increasing lipid accessibility to cat-
alysts, (ii) releasing free ionic Fe from heme proteins, and (iii) in-
hibiting the action of antioxidant enzymes, such as superoxide dis-
mutase, glutathione peroxidase, and catalase (Min, Cordray, & Ahn,
2009). It seems that MRPs can render antioxidant activity and reduce
the prooxidant effect of NaCl in meat products by chelating the liber-
ated ionic iron and inhibiting lipid oxidation.
4.3.5. Dairy products
The improved storage stability of dairy products in the presence of
MRPs has also been reported. McGookin and Augustin (1997) studied
the antioxidative effect of casein-glucose MRPs in full-cream milk
powder and showed that the addition of MRPs retarded the fat oxida-
tion rate, as confirmed by the analysis of peroxide and anisidine indices
and the concentration of headspace volatile compounds. Also, flavor
acceptability of full-cream milk powder reduced more slowly during
storage compared to the control sample. In another study, WPI con-
jugated with D -allose and D -psicose was incorporated into ice-cream.
The product had excellent antioxidative ability (based on the ABTS-RS
activity) and also appropriate quality characteristics, such as overrun
and hardness (Puangmanee, Hayakawa, Sun, & Ogawa, 2008). Ad-
ditionally, milk protein concentrate-sugar blends (sucrose, glucose-
fructose, and glucose-galactose) were used as antioxidants in dairy
beverages containing linseed oil. Results showed that MRPs obtained
from monosaccharides decreased the lipid oxidation of beverage during
sterilization and the concentrations of hexanal and propanal reduced by
100 and 78%, respectively, as the concentration of monosaccharides
reached a final concentration of 0.4 g/100 mL in dairy beverages
(Giroux, Houde, & Britten, 2010).
4.3.6. Edible oils
Direct addition of MRPs into oils, in order to retard or inhibit the
oxidation reaction, has also been successfully reported. Incorporation of
histidine-glucose MRPs retarded autoxidation reaction and peroxide
value of sardine oil, suggesting the role of MRPs as peroxide destroyers
besides autoxidation breakers (Tanaka et al., 1988). Likewise, the oxi-
dation of sardine lipid was effectively inhibited in the presence of
MRPs, prepared by heating tryptophan and glucose, showed a sy-
nergistic effect with natural antioxidant α-tocopherol (Chiu, Tanaka,
Nagashima, & Taguchi, 1991). Similarly, Elizalde, Dalla Rosa, and
Lerici (1991) studied the effect of Maillard reaction volatile products on
the oxidation of soybean oil and reported that the products lengthened
the induction period (3-times) and lowered the oxidation rate at the
propagation stage (50% reduction) and also reduced hexanal formation
compared to the control sample. MRPs have also been successfully
applied for encapsulation of fish and other oils (Augustin, Sanguansri, &
Bode, 2006). In this context, MRPs, particularly protein-polysaccharide
ones can form an impermeable, thick, and viscoelastic interfacial layer
around oil (Nooshkam & Madadlou, 2016b) and other hydrophobic
active bio-compounds. They could provide a physical barrier between
sensitive components and pro-oxidants such as iron, retarding or in-
hibiting their oxidation.
A similar antioxidant activity to phenolic compounds and secondary
antioxidants can be proposed for MRPs, particularly melanoidins
(Fig. 2B). MRPs are able to donate a hydrogen atom (through HAT
mechanism), and neutral free radicals, such as alkyl (R%), alkoxyl (RO%),
and peroxyl (ROO%), are produced during lipid oxidation. It was re-
ported that melanoidins act as chromophores, due to their conjugated
systems (resonance structures), along with electron donating and
M. Nooshkam et al. Food Chemistry 275 (2019) 644–660

withdrawing groups (Moss, 2002). Therefore, the resulted melanoidin

Nicoli, Elizalde, Pitotti, and

Brun-Mérimée et al. (2004)
radicals can be stabilized through delocalizing unpaired electrons in the
conjugated structure, which the obtained radicals can have less re-

Lee and Park (2005)

Billaud et al. (2003)

Billaud et al. (2005)

Mogol et al. (2010)

activity to form new radicals and finally break the free radical chains in

Yuan et al. (2015)

Xu et al. (2016)
the propagation step. As well, melanoidin radicals can scavenge free

Lerici (1991)
radicals and terminate the oxidation reaction. In this way, melanoidins
Reference

can entrap two free radicals via simultaneous hydrogen donation and
electron acceptance. Moreover, melanoidins sequestrate metal ions
such as Fe, which catalyze oxidation reaction and generate free radicals
MRPs showed a partial and direct irreversible inhibition effect through chelating the

Glucose-glycine conjugate showed a non-competitive inhibition effect on potato PPO.

(Fig. 2A). Due to their conjugated structures, melanoidins might also be

MRP and its ultrafiltrate showed comparable inhibitory effects with Na2S2O5 up to
The activity of PPO and POD was reduced nearly to zero in the presence of MRPs.

glucose), in most cases, had similar antibrowning activity to that of metabisulfite.

The Maillard reaction produced MRPs with high inhibitory potency against PPO.

able to quench singlet oxygen like carotenoids. Additionally, melanoi-

Based on the Lineweaver-Burk plot, the MRPs were mixed-type inhibitors, and

MRPs with higher inhibitory efficiency (cysteine-glucose/xylose, glutathione-

dins can regenerate other antioxidants that exist in the system through

MRPs significantly inhibited the enzymatic browning in the food systems as

hydrogen atom donation in a synergistic mode.
glucose-glutathione was more effective than fructose counterpart.

4.3.7. Coffee products

Phenolic compounds participate in the Maillard reaction during
coffee roasting to form water-soluble coffee melanoidins (Borrelli,
MRPs showed inhibitory effect on the enzyme activity.

Visconti, Mennella, Anese, & Fogliano, 2002). The phenolic content

(e.g., chlorogenic acid, ferulic acid, caffeic acid, and p-coumaric acid)
decreased as a consequence of heating during coffee roasting (Delgado-
copper ions in the active site of the enzyme.

Andrade, Rufián-Henares, & Morales, 2005), probably due to con-

confirmed by the color measurement (ΔE).

tributing their carbonyl groups to the Maillard reaction to form phe-

nolic-bound melanoidins. It has been reported that coffee beverages
contain about 25% melanoidins (based on dry matter) and the com-
Antibrowning activity of Maillard reaction products (MRPs) in actual foods (fruits, vegetables, and related products) and model systems.

ponents are responsible for excellent antioxidative capacity and metal-

Impact on enzyme activity

chelating activity, as well as antibacterial and ex vivo protective activ-

ities of the product (Borrelli et al., 2002). Delgado-Andrade et al.
6 h of slice storage.

(2005) found that coffee brew, melanoidins, and bound melanoidin

compounds obtained by ultrafiltration and diafiltration of coffee mel-
anoidins showed high antioxidative capacity in aqueous media. In ad-
dition, the LMW fraction of coffee brews presented greater antioxidant
activity than the HMW fraction. It was demonstrated that coffee mel-
anoidins can be modified by gastrointestinal digestion; LMW com-
pounds released during in vitro digestion presented the highest anti-
Apple purée and potato

oxidative effect compared to those ionically bounded to melanoidins,

eggplant, mushroom
Apple, apple purée,

which was likely attributed to the new structures liberated from mel-
anoidins or improved antioxidant activity of LMW substances non-
Model systems

Model systems

Banana slice
Food systems

covalently (ionically) attached to their structures after digestion. Their

System type

LMW could provide a fast absorption and potential biological activity

cubes

(Rufián-Henares & Morales, 2007a). Furthermore, Borrelli et al. (2002)

reported that the increased intensity of the thermal treatment led to an
increase in the amount of brew melanoidins and decrease in antiradical
Purified from natural sources

PPO and POD (from apple

activity of isolated melanoidins. However, the peroxidation of linoleic

acid was prevented effectively in the dark-roasted samples. In general,
mushroom tyrosinase

PPO (from potato)

coffee melanoidins have some biological roles like antibacterial, anti-

Purified enzyme
Enzyme extract

oxidant, antihypertensive, anti-inflammatory, anticariogenic, and an-

and carrot)
apple PPO
apple PPO

tiglycative activities (Moreira, Nunes, Domingues, & Coimbra, 2012),

Enzyme

which make them potential functional food ingredients for designing

PPO

PPO

PPO

many multi-functional food systems.

5. Antibrowning activity of MRPs

Glutathione and cysteine/galactose, mannose, glucose,
Valine, glycine, serine, cysteine, asparagine, lysine,

5.1. Fruits and vegetables

fructose, arabinose, ribose, and xylose

Enzymatic browning of raw fruits and vegetables is a PPO-catalyzed

oxidation reaction leading to the formation of polymerized dark-co-
arginine, and histidine/glucose

lored pigments from oxidation of o-quinones, which can significantly

Arginine and histidine/glucose
Cysteine/glucose and fructose
Glutathione/glucose, fructose

affect the functional, nutritional, and organoleptic properties of the

product (Mogol, Yıldırım, & Gökmen, 2010). There are some chemical
compounds for inhibiting PPO activity. The most widely studied com-
pounds are halide salts, carboxylic, and other organic acids, as well as
Cysteine/glucose

Cysteine/glucose
Glycine/glucose
Source of MRPs

chelating agents that act on the enzyme. In addition, others are mainly
reducing agents, including ascorbic acid and its derivatives, SH-com-
pounds, and sulfites, which act on the reaction products through o-
Table 3

quinones reduction to o-diphenols (their precursors), and formation of

colorless compounds by reacting with o-quinones (Billaud et al., 2003).

656
M. Nooshkam et al. Food Chemistry 275 (2019) 644–660

Up to now, sulfites are the most effective and cheapest chemical agents time-dependent irreversible and direct inactivation effect of MRPs on
for inhibiting enzymatic browning, but their applications are limited tyrosinase and also showed that the inhibitory effect is partially con-
due to adverse impacts on asthmatic people (Mogol et al., 2010). tributed to by the chelation effect of the compounds towards copper
Therefore, studies dealing with alternative inhibitors of enzymatic ions in the active center of the enzyme. In general, it can be concluded
browning have a great importance. that the chelating activity of MRPs on the enzymes containing copper
The direct inhibition of thiol derivatives through attachment with ions at their active sites, i.e., oxidoreductases such as tyrosinase, POD,
copper at the active site of PPO (copper containing oxidoreductase) has and PPO, is the main reason for the antibrowning effect of the com-
been reported (Brun-Mérimée, Billaud, Louarme, & Nicolas, 2004). pounds produced during the Maillard reaction.
Some studies have shown that MRPs are able to reduce or inhibit the
activity of PPO, peroxidase (POD), and tyrosinase in actual foods
6. Conclusions
(fruits, vegetables, and their products) and model systems (Table 3). For
example, Billaud et al. (2005) studied the effect of MRPs obtained from
In summary, the Maillard reaction can be performed under con-
reacting different monosaccharides and disaccharides with glutathione
trolled conditions via the covalent linkages between components
and cysteine as natural antibrowning agents on PPO activity in apple,
bearing carbonyl and free amino groups without the use of any che-
mushroom, and eggplant. All conjugates inhibited the activity of the
mical compounds. This reaction results in a wide variety of compounds,
enzyme. They also used the MRPs with strong inhibitory effect and
named MRPs which have potential antioxidant, antimicrobial, and an-
minimal color intensity (cysteine-glucose, cysteine-xylose, and glu-
tihypertensive activities and so forth. The different mechanisms for
tathione-glucose conjugates) to evaluate their potential inhibition ef-
antioxidant potency of MRPs like metal chelation, scavenging of free
fects and compared their efficiency with metabisulfite as a common
radicals, breakdown of hydrogen peroxide, and radical chains have
antibrowning agent in real food products, i.e., sliced apple, mushroom,
been proposed by the common and available antioxidative assays.
eggplant, and apple purée (Fig. 3). In apple slices, MRPs, especially
Additionally, these functional compounds have been successfully ap-
cysteine-xylose ones were quite efficient. Browning was not observed in
plied to improve the oxidative stability of diverse foods such as bakery,
eggplant slices in the presence of metabisulfite and MRPs. In mushroom
pasta, meat, oil, and dairy products. As well, they have potential to be
slices, MRPs had the same effect as the metabisulfite. Cysteine-glucose
used as antibrowning agents in place of sulfite compounds, to inhibit
MRPs and metabisulfite showed a similar significant antibrowning ef-
enzymatic browning in fruits and vegetables. Maillard-type conjugates
fect in apple purée. They finally suggested that thiol-derived MRPs can
have some functionality, including improved antioxidant, solubility,
be used as potential sulfite replacers in raw and slightly processed fruits
and heat stability of proteins over a wide range of temperatures, pH
and vegetables (Billaud et al., 2005).
values, and ionic strengths. They also provide a continuous and vis-
In another study, Xu, Zhang, and Karangwa (2016) evaluated the
coelastic layer around oil particles, which make them excellent food-
inhibition effects of MRPs derived from ʟ-cysteine and glucose on en-
grade carriers for the controlled release of biologically active com-
zymatic browning catalyzed by mushroom tyrosinase. They reported a
pounds. It should also be pointed out that separation, purification, and

Fig. 3. Visual appearance of apple (A), eggplant (B), mushroom (C) slices (steeped for 10–15 min), and apple purée (D) treated with MRPs and stored at ambient
temperature for 6 (A and B), 7 (C), and 3 h (D); designed with respect to Billaud et al. (2005).

657
M. Nooshkam et al.
fractionation methods are needed to obtain conjugates for designing
novel delivery systems with boosted functionality. Moreover, the use of
some natural antioxidants such as plant extracts could significantly
reduce the formation of more advanced glycation products without
major influence on early MR products and melanoidins, which are
gaining more attention as potentially bioactive ingredients for food
formulations.
Acknowledgment
The present review was performed at Ferdowsi University of
Mashhad (FUM), Iran.
Conflicts of interest
There are no conflicts of interest to declare.
References
Abdelhedi, O., Mora, L., Jemil, I., Jridi, M., Toldrá, F., Nasri, M., & Nasri, R. (2017). Effect
of ultrasound pretreatment and Maillard reaction on structure and antioxidant
properties of ultrafiltrated smooth-hound viscera proteins-sucrose conjugates. Food
Chemistry, 230, 507–515.
Alfawaz, M., Smith, J. S., & Jeon, I. J. (1994). Maillard reaction products as antioxidants
in pre-cooked ground beef. Food Chemistry, 51(3), 311–318.
Anese, M., Nicoli, M. C., Massini, R., & Lerici, C. R. (1999). Effects of drying processing on
the Maillard reaction in pasta. Food Research International, 32(3), 193–199.
Antony, S. M., Han, I. Y., Rieck, J. R., & Dawson, P. L. (2002). Antioxidative effect of
Maillard reaction products added to turkey meat during heating by addition of honey.
Journal of Food Science, 67(5), 1719–1724.
Augustin, M. A., Sanguansri, L., & Bode, O. (2006). Maillard reaction products as en-
capsulants for fish oil powders. Journal of Food Science, 71(2), 25–32.
Bai, W., Wang, Q., Zeng, X., Fu, J., Liu, Y., & Dong, H. (2017). Antioxidant activities of
chicken peptide-Maillard reaction products (CP-MRPS) derived from chicken pep-
tides and d-glucose system. Journal of Food Processing and Preservation, 41(2), e13041.
Bailey, M. E., & Um, K. W. (1992). Maillard reaction products and lipid oxidation. In A. J.
St Angelo (Ed.). Lipid oxidation in food (pp. 122–139). New York: American Chemical
Society.
Bedinghaus, A. J., & Ockerman, H. W. (1995). Antioxidative Maillard reaction products
from reducing sugars and free amino acids in cooked ground pork patties. Journal of
Food Science, 60(5), 992–995.
Benjakul, S., Lertittikul, W., & Bauer, F. (2005). Antioxidant activity of Maillard reaction
products from a porcine plasma protein–sugar model system. Food Chemistry, 93(2),
189–196.
Billaud, C., Maraschin, C., Chow, Y. N., Chériot, S., Peyrat-Maillard, M. N., & Nicolas, J.
(2005). Maillard reaction products as “natural antibrowning” agents in fruit and
vegetable technology. Molecular Nutrition & Food Research, 49(7), 656–662.
Billaud, C., Roux, E., Brun-Merimee, S., Maraschin, C., & Nicolas, J. (2003). Inhibitory
effect of unheated and heated D -glucose, D-fructose and L-cysteine solutions and
Maillard reaction product model systems on polyphenoloxidase from apple. I.
Enzymatic browning and enzyme activity inhibition using spectrophotometric and
polarographic methods. Food Chemistry, 81(1), 35–50.
Borrelli, R. C., Visconti, A., Mennella, C., Anese, M., & Fogliano, V. (2002). Chemical
characterization and antioxidant properties of coffee melanoidins. Journal of
Agricultural and Food Chemistry, 50(22), 6527–6533.
Bressa, F., Tesson, N., Dalla Rosa, M., Sensidoni, A., & Tubaro, F. (1996). Antioxidant
effect of Maillard reaction products: Application to a butter cookie of a competition
kinetics analysis. Journal of Agricultural and Food Chemistry, 44(3), 692–695.
Brun-Mérimée, S., Billaud, C., Louarme, L., & Nicolas, J. (2004). Effect of glutathione and
Maillard reaction products prepared from glucose or fructose with glutathione on
polyphenoloxidase from apple—II. Kinetic study and mechanism of inhibition. Food
Chemistry, 84(2), 235–241.
Chang, P. S., Lee, J., & Lee, J. L. J. (2005). Development of a new colorimetric method
determining the yield of microencapsulation of α-tocopherol. Journal of Agricultural
and Food Chemistry, 53(19), 7385–7389.
Chawla, S. P., Chander, R., & Sharma, A. (2007). Antioxidant formation by γ-irradiation
of glucose–amino acid model systems. Food Chemistry, 103(4), 1297–1304.
Chawla, S. P., Chander, R., & Sharma, A. (2009). Antioxidant properties of Maillard re-
action products obtained by gamma-irradiation of whey proteins. Food Chemistry,
116(1), 122–128.
Chevalier, F., Chobert, J. M., Genot, C., & Haertlé, T. (2001). Scavenging of free radicals,
antimicrobial, and cytotoxic activities of the Maillard reaction products of β-lacto-
globulin glycated with several sugars. Journal of Agricultural and Food Chemistry,
49(10), 5031–5038.
Chiu, W. K., Tanaka, M., Nagashima, Y., & Taguchi, T. (1991). Prevention of sardine lipid
oxidation by antioxidative Maillard reaction products prepared from fructose-tryp-
tophan. Nippon Suisan Gakaishi, 57, 1773–1781.
de Oliveira, F. C., Coimbra, J. S. D. R., de Oliveira, E. B., Zuñiga, A. D. G., & Rojas, E. E. G.
(2016). Food protein-polysaccharide conjugates obtained via the Maillard reaction: A
review. Critical Reviews in Food Science and Nutrition, 56(7), 1108–1125.
658
Food Chemistry 275 (2019) 644–660
Delgado-Andrade, C., Rufián-Henares, J. A., & Morales, F. J. (2005). Assessing the anti-
oxidant activity of melanoidins from coffee brews by different antioxidant methods.
Journal of Agricultural and Food Chemistry, 53(20), 7832–7836.
Dittrich, R., Dragonas, C., Kannenkeril, D., Hoffmann, I., Mueller, A., Beckmann, M. W., &
Pischetsrieder, M. (2009). A diet rich in Maillard reaction products protects LDL
against copper induced oxidation ex vivo, a human intervention trial. Food Research
International, 42(9), 1315–1322.
Domínguez, R., Gómez, M., Fonseca, S., & Lorenzo, J. M. (2014). Effect of different
cooking methods on lipid oxidation and formation of volatile compounds in foal
meat. Meat Science, 97(2), 223–230.
Dong, S., Wei, B., Chen, B., Mcclements, D. J., & Decker, E. A. (2011). Chemical and
antioxidant properties of casein peptide and its glucose Maillard reaction products in
fish oil-in-water emulsions. Journal of Agricultural and Food Chemistry, 59(24),
13311–13317.
Elizalde, B. E., Dalla Rosa, M., & Lerici, C. R. (1991). Effect of Maillard reaction volatile
products on lipid oxidation. Journal of the American Oil Chemists Society, 68(10), 758.
Fernández, C. L., Fogar, R. A., Doval, M. M., Romero, A. M., & Judis, M. A. (2016).
Antioxidant effect of bovine plasma proteins modified via Maillard reaction on n3
fortified beef patties. Food and Nutrition Sciences, 7(08), 671.
Giroux, H. J., Houde, J., & Britten, M. (2010). Use of heated milk protein–sugar blends as
antioxidant in dairy beverages enriched with linseed oil. LWT-Food Science and
Technology, 43(9), 1373–1378.
Gómez-Ruiz, J.Á., Ames, J. M., & Leake, D. S. (2008). Antioxidant activity and protective
effects of green and dark coffee components against human low density lipoprotein
oxidation. European Food Research and Technology, 227(4), 1017–1024.
González-Mateo, S., González-SanJosé, M. L., & Muñiz, P. (2009). Presence of Maillard
products in Spanish muffins and evaluation of colour and antioxidant potential. Food
and Chemical Toxicology, 47(11), 2798–2805.
Gu, F. L., Kim, J. M., Abbas, S., Zhang, X. M., Xia, S. Q., & Chen, Z. X. (2010). Structure
and antioxidant activity of high molecular weight Maillard reaction products from
casein–glucose. Food Chemistry, 120(2), 505–511.
Gu, F., Kim, J. M., Hayat, K., Xia, S., Feng, B., & Zhang, X. (2009). Characteristics and
antioxidant activity of ultrafiltrated Maillard reaction products from a casein–glucose
model system. Food Chemistry, 117(1), 48–54.
Gupta, R. K., Gupta, K., Sharma, A., Das, M., Ansari, I. A., & Dwivedi, P. D. (2018).
Maillard reaction in food allergy: Pros and cons. Critical Reviews in Food Science and
Nutrition, 58(2), 208–226.
Hamdani, A. M., Wani, I. A., Bhat, N. A., & Siddiqi, R. A. (2018). Effect of guar gum
conjugation on functional, antioxidant and antimicrobial activity of egg white lyso-
zyme. Food Chemistry, 240, 1201–1209.
Han, M. M., Yi, Y., Wang, H. X., & Huang, F. (2017). Investigation of the Maillard reaction
between polysaccharides and proteins from longan pulp and the improvement in
activities. Molecules, 22(6), 938.
Hwang, I. G., Kim, H. Y., Woo, K. S., Lee, J., & Jeong, H. S. (2011). Biological activities of
Maillard reaction products (MRPs) in a sugar–amino acid model system. Food
Chemistry, 126(1), 221–227.
Jiang, Z., & Brodkorb, A. (2012). Structure and antioxidant activity of Maillard reaction
products from α-lactalbumin and β-lactoglobulin with ribose in an aqueous model
system. Food Chemistry, 133(3), 960–968.
Jiang, Z., Rai, D. K., O’Connor, P. M., & Brodkorb, A. (2013). Heat-induced Maillard
reaction of the tripeptide IPP and ribose: Structural characterization and implication
on bioactivity. Food Research International, 50(1), 266–274.
Jiménez-Zamora, A., Pastoriza, S., & Rufián-Henares, J. A. (2015). Revalorization of
coffee by-products. Prebiotic, antimicrobial and antioxidant properties. LWT-Food
Science and Technology, 61(1), 12–18.
Karbasi, M., & Madadlou, A. (2018). Interface-related attributes of the Maillard reaction-
born glycoproteins. Critical Reviews in Food Science and Nutrition, 58(10), 1595–1603.
Karnjanapratum, S., Benjakul, S., & O’Brien, N. (2017). Production of antioxidative
Maillard reaction products from gelatin hydrolysate of unicorn leatherjacket skin.
Journal of Aquatic Food Product Technology, 26(2), 148–162.
Khadidja, L., Asma, C., Mahmoud, B., & Meriem, E. (2017). Alginate/gelatin crosslinked
system through Maillard reaction: Preparation, characterization and biological
properties. Polymer Bulletin, 74(12), 4899–4919.
Kim, J. S., & Lee, Y. S. (2009). Antioxidant activity of Maillard reaction products derived
from aqueous glucose/glycine, diglycine, and triglycine model systems as a function
of heating time. Food Chemistry, 116(1), 227–232.
Kitts, D. D., & Hu, C. (2005). Biological and chemical assessment of antioxidant activity of
sugar-lysine model maillard reaction products. Annals of the New York Academy of
Sciences, 1043(1), 501–512.
Lee, M. K., & Park, I. (2005). Inhibition of potato polyphenol oxidase by Maillard reaction
product. Food Chemistry, 91(1), 57–61.
Lee, Y. Y., Tang, T. K., Phuah, E. T., Alitheen, N. B. M., Tan, C. P., & Lai, O. M. (2017).
New functionalities of maillard reaction products as emulsifier and encapsulating
agent and its processing parameters: A brief review. Journal of the Science of Food and
Agriculture, 97, 1379–1385.
Lertittikul, W., Benjakul, S., & Tanaka, M. (2007). Characteristics and antioxidative ac-
tivity of Maillard reaction products from a porcine plasma protein–glucose model
system as influenced by pH. Food Chemistry, 100(2), 669–677.
Li, X., Shi, X., Jin, Y., Ding, F., & Du, Y. (2013). Controllable antioxidative xylan–chitosan
Maillard reaction products used for lipid food storage. Carbohydrate Polymers, 91(1),
428–433.
Lin, C., Toto, C., & Were, L. (2015). Antioxidant effectiveness of ground roasted coffee in
raw ground top round beef with added sodium chloride. LWT-Food Science and
Technology, 60(1), 29–35.
Lingnert, H. (1980). Antioxidative Maillard reaction products III. Application in cookies.
Journal of Food Processing and Preservation, 4(4), 219–233.
M. Nooshkam et al.
Lingnert, H., & Eriksson, C. E. (1980). Antioxidative Maillard reaction products. II.
Products from sugars and peptides or protein hydrolysates. Journal of Food Processing
and Preservation, 4(3), 173–181.
Lingnert, H., & Lundgren, B. (1980). Antioxidative Maillard reaction products IV.
Application in sausage. Journal of Food Processing and Preservation, 4(4), 235–246.
Liu, Q., Li, J., Kong, B., Jia, N., & Li, P. (2014). Antioxidant capacity of Maillard reaction
products formed by a porcine plasma protein hydrolysate-sugar model system as
related to chemical characteristics. Food Science and Biotechnology, 23(1), 33–41.
Losso, J. N. (2016). The Maillard reaction reconsidered: cooking and eating for health. CRC
Press.
Martín, M. A., Ramos, S., Mateos, R., Rufián-Henares, J. A., Morales, F. J., Bravo, L., &
Goya, L. (2009). Biscuit melanoidins of different molecular masses protect human
HepG2 cells against oxidative stress. Journal of Agricultural and Food Chemistry,
57(16), 7250–7258.
Martinez-Alvarenga, M. S., Martinez-Rodriguez, E. Y., Garcia-Amezquita, L. E., Olivas, G.
I., Zamudio-Flores, P. B., Acosta-Muniz, C. H., & Sepulveda, D. R. (2014). Effect of
Maillard reaction conditions on the degree of glycation and functional properties of
whey protein isolate–Maltodextrin conjugates. Food Hydrocolloids, 38, 110–118.
Martins, S. I., Jongen, W. M., & Van Boekel, M. A. (2000). A review of Maillard reaction in
food and implications to kinetic modelling. Trends in Food Science & Technology,
11(9), 364–373.
McGookin, B. J., & Augustin, M. A. (1997). Antioxidant activity of a heated casein-glucose
mixture in full-cream milk powder. Australian Journal of Dairy Technology, 52(1),
15–19.
Mengíbar, M., Miralles, B., & Heras, Á. (2017). Use of soluble chitosans in Maillard re-
action products with β-lactoglobulin. Emulsifying and antioxidant properties. LWT-
Food Science and Technology, 75, 440–446.
Michalska, A., Amigo-Benavent, M., Zielinski, H., & del Castillo, M. D. (2008). Effect of
bread making on formation of Maillard reaction products contributing to the overall
antioxidant activity of rye bread. Journal of Cereal Science, 48(1), 123–132.
Min, B., Cordray, J. C., & Ahn, D. U. (2009). Effect of NaCl, myoglobin, Fe (II), and Fe (III)
on lipid oxidation of raw and cooked chicken breast and beef loin. Journal of
Agricultural and Food Chemistry, 58(1), 600–605.
Miranda, L. T., Rakovski, C., & Were, L. M. (2012). Effect of Maillard reaction products on
oxidation products in ground chicken breast. Meat Science, 90(2), 352–360.
Mogol, B. A., Yıldırım, A., & Gökmen, V. (2010). Inhibition of enzymatic browning in
actual food systems by the Maillard reaction products. Journal of the Science of Food
and Agriculture, 90(15), 2556–2562.
Morales, F. J., Fernández-Fraguas, C., & Jiménez-Pérez, S. (2005). Iron-binding ability of
melanoidins from food and model systems. Food Chemistry, 90(4), 821–827.
Morales, F. J., & Jiménez-Pérez, S. (2004). Peroxyl radical scavenging activity of mela-
noidins in aqueous systems. European Food Research and Technology, 218(6), 515–520.
Moreira, A. S., Nunes, F. M., Domingues, M. R., & Coimbra, M. A. (2012). Coffee mela-
noidins: Structures, mechanisms of formation and potential health impacts. Food &
Function, 3(9), 903–915.
Moss, B. W. (2002). The chemistry of food colour. In D. B. MacDougall (Ed.). Colour in
food: Improving quality (pp. 145–178). Cambridge: Woodhead Publishing Limited and
CRC Press LLC.
Nasrollahzadeh, F., Varidi, M., Koocheki, A., & Hadizadeh, F. (2017). Effect of microwave
and conventional heating on structural, functional and antioxidant properties of
bovine serum albumin-maltodextrin conjugates through Maillard reaction. Food
Research International, 100, 289–297.
Nicoli, M. C., Elizalde, B. E., Pitotti, A., & Lerici, C. R. (1991). Effect of sugars and
maillard reaction products on polyphenol oxidase and peroxidase activity in food.
Journal of Food Biochemistry, 15(3), 169–184.
Nie, X., Zhao, L., Regenstein, J. M., Xu, D., & Meng, X. (2017). Antioxidant capacity of
Maillard reaction products’ fractions with different molecular weight distribution
from chicken bone hydrolysate–galactose system. International Journal of Food Science
& Technology, 52(7), 1632–1638.
Nooshkam, M., Babazadeh, A., & Jooyandeh, H. (2018). Lactulose: Properties, techno-
functional food applications, and food grade delivery system. Trends in Food Science &
Technology, 80, 23–34.
Nooshkam, M., & Madadlou, A. (2016a). Maillard conjugation of lactulose with poten-
tially bioactive peptides. Food Chemistry, 192, 831–836.
Nooshkam, M., & Madadlou, A. (2016b). Microwave-assisted isomerisation of lactose to
lactulose and Maillard conjugation of lactulose and lactose with whey proteins and
peptides. Food Chemistry, 200, 1–9.
Nursten, H. E. (2005). The Maillard reaction: Chemistry, biochemistry, and implications.
Royal Society of Chemistry.
O’Brien, J., Morrissey, P. A., & Ames, J. M. (1989). Nutritional and toxicological aspects
of the Maillard browning reaction in foods. Critical Reviews in Food Science & Nutrition,
28(3), 211–248.
Pastoriza, S., & Rufián-Henares, J. A. (2014). Contribution of melanoidins to the anti-
oxidant capacity of the Spanish diet. Food Chemistry, 164, 438–445.
Patrignani, M., Rinaldi, G. J., & Lupano, C. E. (2016). In vivo effects of Maillard reaction
products derived from biscuits. Food Chemistry, 196, 204–210.
Peng, X., Ma, J., Chen, F., & Wang, M. (2011). Naturally occurring inhibitors against the
formation of advanced glycation end-products. Food & Function, 2(6), 289–301.
Perusko, M., Al-Hanish, A., Velickovic, T. C., & Stanic-Vucinic, D. (2015).
Macromolecular crowding conditions enhance glycation and oxidation of whey
proteins in ultrasound-induced Maillard reaction. Food Chemistry, 177, 248–257.
Poulsen, M. W., Hedegaard, R. V., Andersen, J. M., de Courten, B., Bügel, S., Nielsen, J., ...
Dragsted, L. O. (2013). Advanced glycation endproducts in food and their effects on
health. Food and Chemical Toxicology, 60, 10–37.
Puangmanee, S., Hayakawa, S., Sun, Y., & Ogawa, M. (2008). Application of whey protein
isolate glycated with rare sugars to ice cream. Food Science and Technology Research,
659
Food Chemistry 275 (2019) 644–660
14(5) 457-457.
Rao, M. S., Chawla, S. P., Chander, R., & Sharma, A. (2011). Antioxidant potential of
Maillard reaction products formed by irradiation of chitosan–glucose solution.
Carbohydrate Polymers, 83(2), 714–719.
Rufian-Henares, J. A., & De la Cueva, S. P. (2008). Assessment of hydroxymethylfurfural
intake in the Spanish diet. Food Additives and Contaminants, 25(11), 1306–1312.
Rufián-Henares, J.Á., García-Villanova, B., & Guerra-Hernández, E. (2004). Generation of
furosine and color in infant/enteral formula-resembling systems. Journal of
Agricultural and Food Chemistry, 52(17), 5354–5358.
Rufián-Henares, J.Á., Guerra-Hernández, E., & García-Villanova, B. (2004). Pyrraline
content in enteral formula processing and storage and model systems. European Food
Research and Technology, 219(1), 42–47.
Rufián-Henares, J. A., & Morales, F. J. (2007a). Effect of in vitro enzymatic digestion on
antioxidant activity of coffee melanoidins and fractions. Journal of Agricultural and
Food Chemistry, 55(24), 10016–10021.
Rufián-Henares, J. A., & Morales, F. J. (2007b). Functional properties of melanoidins: In
vitro antioxidant, antimicrobial and antihypertensive activities. Food Research
International, 40(8), 995–1002.
Ruiz-Roca, B., Navarro, M. P., & Seiquer, I. (2008). Antioxidant properties and metal
chelating activity of glucose-lysine heated mixtures: Relationships with mineral ab-
sorption across Caco-2 cell monolayers. Journal of Agricultural and Food Chemistry,
56(19), 9056–9063.
Schwarzenbolz, U., Hofmann, T., Sparmann, N., & Henle, T. (2016). Free Maillard reac-
tion products in milk reflect nutritional intake of glycated proteins and can be used to
distinguish “organic” and “conventionally” produced milk. Journal of Agricultural and
Food Chemistry, 64(24), 5071–5078.
Seifert, S. T., Krause, R., Gloe, K., & Henle, T. (2004). Metal complexation by the peptide-
bound Maillard reaction products N ε-fructoselysine and N ε-carboxymethyllysine.
Journal of Agricultural and Food Chemistry, 52(8), 2347–2350.
Seiquer, I., Ruiz-Roca, B., Mesías, M., Muñoz-Hoyos, A., Galdó, G., Ochoa, J. J., &
Navarro, M. P. (2008). The antioxidant effect of a diet rich in Maillard reaction
products is attenuated after consumption by healthy male adolescents. In vitro and in
vivo comparative study. Journal of the Science of Food and Agriculture, 88(7),
1245–1252.
Serpen, A., & Gökmen, V. (2009). Evaluation of the Maillard reaction in potato crisps by
acrylamide, antioxidant capacity and color. Journal of Food Composition and Analysis,
22(6), 589–595.
Shahidi, F. (2000). Antioxidants in food and food antioxidants. Food/Nahrung, 44(3),
158–163.
Shahidi, F., & Zhong, Y. (2010). Lipid oxidation and improving the oxidative stability.
Chemical Society Reviews, 39(11), 4067–4079.
Silván, J. M., Assar, S. H., Srey, C., del Castillo, M. D., & Ames, J. M. (2011). Control of the
Maillard reaction by ferulic acid. Food Chemistry, 128(1), 208–213.
Song, R., Shi, Q., Yang, P., & Wei, R. (2018). In vitro membrane damage induced by half-
fin anchovy hydrolysates/glucose Maillard reaction products and the effects on oxi-
dative status in vivo. Food & function, 9(2), 785–796.
Song, R., Yang, P., Wei, R., & Ruan, G. (2016). Antioxidative, antibacterial, and food
functional properties of the half-fin anchovy hydrolysates-glucose conjugates formed
via Maillard reaction. Molecules, 21(6), 795.
Sproston, M. J., & Akoh, C. C. (2016). Antioxidative effects of a glucose-cysteine Maillard
reaction product on the oxidative stability of a structured lipid in a complex food
emulsion. Journal of Food Science, 81(12), C1–C9.
Su, G., Zheng, L., Cui, C., Yang, B., Ren, J., & Zhao, M. (2011). Characterization of an-
tioxidant activity and volatile compounds of Maillard reaction products derived from
different peptide fractions of peanut hydrolysate. Food Research International, 44(10),
3250–3258.
Sun, Y., Hayakawa, S., Chuamanochan, M., Fujimoto, M., Innun, A., & Izumori, K. (2006).
Antioxidant effects of Maillard reaction products obtained from ovalbumin and dif-
ferent D-aldohexoses. Bioscience, Biotechnology, and Biochemistry, 70(3), 598–605.
Sun, Y., Hayakawa, S., & Izumori, K. (2004). Antioxidative activity and gelling rheolo-
gical properties of dried egg white glycated with a rare keto-hexose through the
Maillard reaction. Journal of Food Science, 69(6), C427–C434.
Sun, Y., Hayakawa, S., Ogawa, M., Fukada, K., & Izumori, K. (2008). Influence of a rare
sugar, D-psicose, on the physicochemical and functional properties of an aerated food
system containing egg albumen. Journal of Agricultural and Food Chemistry, 56(12),
4789–4796.
Sun, Y., Hayakawa, S., Puangmanee, S., & Izumori, K. (2006). Chemical properties and
antioxidative activity of glycated α-lactalbumin with a rare sugar, D-allose, by
Maillard reaction. Food Chemistry, 95(3), 509–517.
Tanaka, M., Kuei, C. W., Nagashima, Y., & Taguchi, T. (1988). Application of anti-
oxidative Maillard reaction products from histidine and glucose to sardine products.
Nippon Suisan Gakkaishi, 54(8), 1409–1414.
Uribarri, J., Woodruff, S., Goodman, S., Cai, W., Chen, X., Pyzik, R., ... Vlassara, H.
(2010). Advanced glycation end products in foods and a practical guide to their re-
duction in the diet. Journal of the American Dietetic Association, 110(6), 911–916.
Van Nguyen, C. (2006). Toxicity of the AGEs generated from the Maillard reaction: On the
relationship of food-AGEs and biological-AGEs. Molecular Nutrition & Food Research,
50(12), 1140–1149.
Vhangani, L. N., & Van Wyk, J. (2013). Antioxidant activity of Maillard reaction products
(MRPs) derived from fructose–lysine and ribose–lysine model systems. Food
Chemistry, 137(1), 92–98.
Vhangani, L. N., & Van Wyk, J. (2016). Antioxidant activity of Maillard reaction products
(MRPs) in a lipid-rich model system. Food Chemistry, 208, 301–308.
Wang, W. Q., Bao, Y. H., & Chen, Y. (2013). Characteristics and antioxidant activity of
water-soluble Maillard reaction products from interactions in a whey protein isolate
and sugars system. Food Chemistry, 139(1), 355–361.
M. Nooshkam et al.
Wang, H. Y., Qian, H., & Yao, W. R. (2011). Melanoidins produced by the Maillard re-
action: Structure and biological activity. Food Chemistry, 128(3), 573–584.
Wijewickreme, A. N., Kitts, D. D., & Durance, T. D. (1997). Reaction conditions influence
the elementary composition and metal chelating affinity of nondialyzable model
Maillard reaction products. Journal of Agricultural and Food Chemistry, 45(12),
4577–4583.
Xu, H., Zhang, X., & Karangwa, E. (2016). Inhibition effects of Maillard reaction products
derived from L-cysteine and glucose on enzymatic browning catalyzed by mushroom
tyrosinase and characterization of active compounds by partial least squares re-
gression analysis. RSC Advances, 6(70), 65825–65836.
Yan, F., Yu, X., & Jing, Y. (2018). Optimized preparation, characterization, and anti-
oxidant activity of chitooligosaccharide–glycine Maillard reaction products. Journal
of Food Science and Technology, 55(2), 712–720.
Yáñez, D. A. C., Gagneten, M., Leiva, G. E., & Malec, L. S. (2018). Antioxidant activity
developed at the different stages of Maillard reaction with milk proteins. LWT-Food
Science and Technology, 89, 344–349.
Yen, G. C., & Hsieh, P. P. (1995). Antioxidative activity and scavenging effects on active
oxygen of xylose-lysine maillard reaction products. Journal of the Science of Food and
660
Food Chemistry 275 (2019) 644–660
Agriculture, 67(3), 415–420.
Yilmaz, Y., & Toledo, R. (2005). Antioxidant activity of water-soluble Maillard reaction
products. Food Chemistry, 93(2), 273–278.
Yoshimura, Y., Iijima, T., Watanabe, T., & Nakazawa, H. (1997). Antioxidative effect of
Maillard reaction products using glucose− glycine model system. Journal of
Agricultural and Food Chemistry, 45(10), 4106–4109.
Yu, M., He, S., Tang, M., Zhang, Z., Zhu, Y., & Sun, H. (2018). Antioxidant activity and
sensory characteristics of Maillard reaction products derived from different peptide
fractions of soybean meal hydrolysate. Food Chemistry, 243, 249–257.
Yuan, D., Xu, Y., Wang, C., Li, Y., Li, F., Zhou, Y., ... Jiang, Y. (2015). Comparison of anti-
browning ability and characteristics of the fractionated Maillard reaction products
with different polarities. Journal of Food Science and Technology, 52(11), 7163–7172.
Zhong, N. J., Liu, G. Q., Zhao, X. H., Gao, Y. Q., Li, L., & Li, B. (2015). Lipid peroxidation
inhibitation activity of Maillard reaction products derived from sugar-amino acid
model systems. Advance Journal of Food Science and Technology, 9(5), 393–397.
Zhu, K. X., Li, J., Li, M., Guo, X. N., Peng, W., & Zhou, H. M. (2013). Functional properties
of chitosan–xylose Maillard reaction products and their application to semi-dried
noodle. Carbohydrate Polymers, 92(2), 1972–1977.