Critical Reviews in Food Science and Nutrition, 45:49–59 (2005)

Copyright
C Taylor and Francis Inc.

ISSN: 1040-8398
DOI: 10.1080/10408690590900117

Coordinate Contribution of Lipid

Oxidation and Maillard Reaction to
the Nonenzymatic Food Browning
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ROSARIO ZAMORA and FRANCISCO J. HIDALGO

Instituto de la Grasa, Consejo Superior de Investigaciones Cientı́ficas, Sevilla, Spain

Lipid oxidation and the Maillard reaction are probably the two most important reactions in Food Science. Both include a whole
network of different reactions in which an extraordinary complex mixture of compounds are obtained in very different amounts
and produce important changes in food flavor, color, texture, and nutritional value, with positive and negative consequences.
This article analyzes the interactions between both reactions, with special emphasis in nonenzymatic browning development,
by discussing the influence of lipid oxidation products in the Maillard pathway and vice versa, as well as the existence of
common intermediates and polymerization mechanisms in both reactions. The existing data suggest that both reactions are
so interrelated that they should be considered simultaneously to understand the products of the Maillard reaction in the
presence of lipids and vice versa, and should be included in one general pathway that can be initiated by both lipids and
carbohydrates.

Keywords Food antioxidants, food colors, food processing, food quality, lipid oxidation, Maillard reaction, nonenzymatic
browning

INTRODUCTION of foods may be modified by a series of reactions among food

Color is often the first sensory quality by which foods are
judged, and it may also provide an indication of the chemical
changes suffered by them. Food colors are the result of a vari-
ety of factors, both endogenous and exogenous to the food that
may be effected by genetics and pre- and postharvested treat-
ments. The exogenous factors consist of such things as packag-
ing films, display lights, and processing, while the endogenous
factors involve pigments within the food, added colors, and phys-
ical characteristics that affect glossiness and haze (Clydesdale,
1988; Francis, 1993; MacDougall, 2002).
With few exceptions, natural food pigments can be divided
into four groups: tetrapyrrole compounds (chlorophylls, hemes,
and bilins), isoprenoid derivatives (carotenoids), benzopyran
derivatives (anthocyanins and flavonoids), and betanidin deriva-
tives (betalains) (Belitz and Grosch, 1999; Boileau et al., 1999;
Delgado-Vargas et al., 2000; von Elbe and Schwartz, 1996;
Francis, 1985; Hendrich et al., 1999; Hendry and Houghton,
1996; MacDougall, 2002; deMan, 1999; Mı́nguez et al., 1999;
Shahidi et al., 1998). In addition to natural pigments, the color
Address correspondence to Dr. Francisco J. Hidalgo, Instituto de la
Grasa, Avenida Padre Garcı́a Tejero 4, 41012 Sevilla, Spain. E-mail:
fhidalgo@ig.csic.es
49
constituents that produce the consequence commonly termed as
food browning (Friedman, 1996; Sapers, 1993).
Food browning is mostly the consequence of a series of re-
actions of amines, amino acids, peptides, and proteins with re-
ducing sugars, oxidized lipids, vitamin C, and quinones. The
reaction with quinones is known as enzymatic browning, be-
cause the quinones are usually produced enzymatically from
phenols, and the others are grouped as nonenzymatic brown-
ing reactions. Although the nonenzymatic oxidation of phenols
has also been described after alkaline treatments, this reaction is
thought to produce browning by similar mechanisms to the enzy-
matic browning (Hurrell and Finot, 1985; Finot, 1997; Mauron,
1986).
Browning reactions in foods are more complex than is
suggested by the simple classification of these reactions as en-
zymatic or nonenzymatic, because of the large number of sec-
ondary reactions that may occur. For example, pre-peeled
potatoes may develop red, brown, or even black discolorations,
sometimes on opposite sides of the same tuber (Feinberg et al.,
1987). These discolorations are the result of enzymatic brown-
ing reactions, but nonenzymatic “after cooking darkening”, in-
duced by heating during steam or lye peeling, also may con-
tribute to discoloration of the peeled surface (Smith, 1987).
Discolorations may also occur in some raw products in which
 50 R. ZAMORA AND F. J. HIDALGO

endogenous or added ascorbic acid is oxidized to dehydroascor-

bic acid, which then reacts with amino acids to yield brown
colors by the Maillard reaction or other nonenzymatic means
(Kacem et al., 1987). These are only some examples that illus-
trate how all these reactions are interrelated and, sometimes, a
specific effect is the consequence of several reactions.
Although the different reactions that produce food brown-
ing have been broadly reviewed, the interactions among them
are scarcely found in the literature. In an attempt to update
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the diverse studies carried out in recent years in this field, this
article reviews the interactions in the nonenzymatic browning
produced as a consequence of lipid oxidation and the Maillard
reaction.

NONENZYMATIC BROWNING PRODUCED AS A

CONSEQUENCE OF THE MAILLARD REACTION

The Maillard reaction is the nonenzymatic glycosidation of

amino acids or proteins to form glycated products. It embraces
a whole network of different reactions in which an extraordi-
nary complex mixture of compounds are obtained in very dif-
ferent amounts. In foods, this reaction takes place essentially
between the monosaccharides, glucose and fructose, or the dis-
accharides, maltose and lactose, as well as in some cases (e.g.,
meat) reducing pentoses, and amino acids and/or proteins. Al-
though carbohydrate oxidation is also produced to some extent,
the first step of the Maillard reaction is generally accepted to be
the formation of a N -substituted glycosylamine from an aldose
(or ketose) reacting with a primary amino group of an amino
acid, peptide, or protein. This glycosylamine then suffers an
Amadori rearrangement type of reaction to yield a 1-amino-1-
deoxy-2-ketose. The next step of the reaction is the dehydration,
fragmentation, or enolization of the sugar, or the Strecker degra-
dation to produce both amino or nonamino compounds. Finally,
the condensation of some of the products formed in this step is
produced either among them or with amino compounds to form
brown pigments and polymers (Danehy, 1986; Deyl and Miksik,
1997; Hasenkopf et al., 2002; Hodge, 1953; Hurst, 1972; Ikan,
1996; Labuza and Baisier, 1992; Ledl and Schleicher, 1990;
Namiki, 1988; O’Brien et al., 1998). Figure 1 summarizes these
reactions.
If the reaction mixtures of sugars and amines are submit-
ted to exclusion chromatography, fractions can be obtained with
molecular weights of about 7000 Da and even greater, and these
fractions are predominant (>95% p. w.) (Tressl et al., 1998a).
However, so far it has not yet proved possible to isolate ho-
mogeneous high molecular weight Maillard products, and very
little is known about the structure of these products, the so-
called melanoidins. In addition, 1 H and 13 C-NMR spectra of the
melanoidins isolated by different research groups differed sub-
stantially, and melanoidins with groups of signals that largely re-
semble those of Amadori compounds (Kato and Tsuchida, 1981;
Olsson et al., 1981) contrast with those that exhibit signals in
the olefin, aromatic, and carbonyl regions (Benzing-Purdie and
Figure 1 The Maillard reaction pathway.
Ratcliffe, 1986; Feather and Huang, 1986; Huang and Feather,
1988; Kato et al., 1986). These results seem to indicate both a
variety of melanoidin structures and the difficulty to purify these
polymers that can absorb monomers; these last compounds are
probably appearing in the spectra. Additional studies with 15 N-
labeled amino acids showed that the melanoidins obtained ex-
hibited signals in the pyrrole, indole, and amide region of the
15
N-NMR spectrum (Benzing-Purdie and Ratcliffe, 1986).
NONENZYMATIC BROWNING PRODUCED AS
A CONSEQUENCE OF THE LIPID OXIDATION
The role of lipids in the nonenzymatic browning reactions
is a consequence of their liability to be oxidized (Hidalgo and
Zamora, 2000a). Autoxidation of fats is the main reaction in-
volved in the oxidative deterioration of lipids, although in foods,
the lipids can be oxidized by both enzymatic and nonenzymatic
mechanisms. Nonenzymatic oxidation or autoxidation of fats
proceeds via typical free radical mechanisms and hydroperox-
ides are the initial products. They are relatively unstable and en-
ter into numerous complex reactions involving substrate degra-
dation and interaction, resulting in a myriad of compounds of
various molecular weights, flavor thresholds, and biological sig-
nificance (Berdeaux et al., 1999; Erickson, 2002; Frankel, 1998;
 LIPID OXIDATION AND MAILLARD REACTION TO FOOD BROWNING
Gasparoli, 1998; Guillen-Sans and Guzman-Chozas, 1998;
Hidalgo and Zamora, 2002; Kamal-Eldin and Appelqvist, 1996;
Min and Boff, 2002; Nawar, 1996, 1998).
Although lipid oxidation products may polymerize to pro-
duce brown-colored oxypolymers (Buttkus, 1975; Khayat and
Schwall, 1983; Venolia and Tappel, 1958), in the presence of
other compounds (e.g., proteins, antioxidants, etc.), oxidative re-
actions (both enzymatic and nonenzymatic) can be terminated by
reactions with compounds other than those originating from oxi-
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dation of the lipid substrate; this can influence reaction rates and
produce significant consequences in the color, flavor, and texture
of foods. Particularly, the reaction of lipid oxidation products
with amines, amino acids, and proteins has long been related to
both the browning observed in many fatty foods during process-
ing and storage (El-Zeany and Fattah, 1982; Gillatt and Rossell,
1992; Hidalgo and Zamora, 2000b; Pokorny, 1998; Stansby,
1957) and the progressive accumulation of age-related yellow-
brown pigments (lipofuscins) in man and animals (Miquel et
al., 1977; Porta and Hartroff, 1969; Sohal, 1981; Strehler, 1964;
Yin, 1996). In addition, a direct relationship between fluores-
cence and browning has been found in diverse studies (Adhikari
and Tappel, 1973; Hidalgo and Zamora, 1993a). Figure 2 sum-
marizes these reactions.
Figure 2 The lipid oxidation pathway.
51
LIPID OXIDATION AND THE MAILLARD REACTION
Lipid oxidation and the Maillard reaction are probably the
two most important reactions in Food Science. Both include
a whole network of different reactions in which an extraordi-
nary complex mixture of compounds are obtained in very dif-
ferent amounts and produce important changes in food flavor,
color, texture, and nutritional value, with positive and nega-
tive consequences. In addition, as observed in Figures 1 and
2, and from a nonenzymatic browning point of view, both reac-
tions follow similar general reaction pathways. Both have one
key compound that is formed in a first step (lipid hydroperoxides
in lipid oxidation, and Amadori compounds in the
Maillard reaction), and the later fragmentation, rearrangement,
degradation, etc., of these compounds produce a number of
volatiles and nonvolatile monomers in a second step. These
compounds are responsible for the production of highly col-
ored polymers by aldol condensations and/or carbonyl-amine
polymerization.
This gross similarity between both reactions has made dif-
ferent groups question the independence of these two reactions
and investigate how one reaction may influence the other, as
well as the existence of common intermediates and/or mecha-
nisms that produce similar browned products from both lipids
and carbohydrates.
Role of Maillard Reaction Products in the Lipid
Oxidation Pathway
Maillard reaction products have been described to both pro-
mote and reduce lipid oxidation (Ames, 2001). Thus, Amadori
products have been shown to increase phospholipid oxidation.
Breitling-Utzmann et al. (2001) studied the oxidation of soybean
phosphatidylethanolamine induced by a synthetically prepared
Amadori product of phosphatidylethanolamine. This derivative
increased TBARS production in soybean phosphatidylethanola-
mine when incubated in vitro, with respect to the same phospho-
lipid incubated in the presence of the phosphatidylethanolamine
employed in the preparation of the Amadori product, which was
used as a control. These results also confirm the data found by
Bucala et al. (1993), who suggested that phospholipid glycation
enhanced lipid peroxidation.
On the contrary, many other Maillard reaction products,
including nonenzymatically browned proteins, are well docu-
mented to reduce lipid oxidation. Alaiz et al. (1999), for exam-
ple, incubated BSA with ribose for 24 h at different temperatures
and produced a browned protein with a potent antioxidant activ-
ity in the protection of vegetable oils. This antioxidant activity
was parallel to the browning produced in the protein and was in-
versely correlated with the lysine recovered after acid hydrolysis.
Analogous effects have also been found in many other studies
(Arnoldi, 1990; Chuyen, 1998; Chuyen et al., 1998; Farag et al.,
1982; Franzke and Iwainsky, 1954; Morales and Babbel, 2002;
Park and Kim, 1983; Wijewickreme and Kitts, 1998), including
 52 R. ZAMORA AND F. J. HIDALGO
in vivo studies (Chuyen et al., 1990). Similar antioxidant
activities were also found for nonenzymatically browned pro-
teins produced as a consequence of lipid oxidation (Ahmad et al.,
1998; Alaiz et al., 1997a, 1998; Hidalgo et al., 2001; Zamora
et al., 1997).
Role of Lipid Oxidation Products in the Maillard
Reaction Pathway
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Analogously to the influence of Maillard products in the lipid
oxidation pathway, lipid oxidation products are also able to mod-
ify Maillard reaction by promoting the reaction or by reacting
with some intermediates and producing compounds different to
those commonly formed in the absence of lipids. One example of
this is the development of aroma in cooked meat, where the pres-
ence of lipids is essential to get the pleasant flavors (Gandemer,
1999; Mottram and Edwards, 1983). Mottram and colleagues de-
veloped a meat-like model system consisting of an amino acid
(mainly cysteine or methionine) and ribose in a phosphate buffer
to which they added various phospholipid moieties or phospho-
lipids. From these studies, it was concluded that lipids interact
in Maillard reactions both by the amino group of the polar head
of phospholipids and by some of the oxidative breakdown prod-
ucts of fatty acids, such as aldehydes. Hence, lipids contribute
to meat aroma improvement both by reducing the amount of
sulfur-containing compounds and by providing volatiles, such
as carbonyls or alcohols. The most likely mechanism for the re-
duction of sulfur-containing heterocyclic volatiles could be reac-
tions between aldehydes from fatty acid oxidation and hydrogen
sulfide, reducing the availability of this key compound for the
formation of sulfur heterocyclics. The quenching of the forma-
tion of Maillard reaction products is more pronounced when
the meat contains a high proportion of polyunsaturated fatty
acids (MacLeod and Seyyedain-Ardebili, 1981; Meynier and
Gandemer, 1994), therefore, suggesting that the more favored
the lipid oxidation, the more affected the Maillard reaction
pathway.
Another example in this sense was found by Negroni et al.
(2001) when studying the effects of olive, canola, and sun-
flower oils on the formation of volatiles from the Maillard re-
action of lysine with xylose and glucose. Pyrazine production
appeared to be particularly sensitive to the degree of unsatura-
tion of the oils in both xylose-lysine and glucose-lysine model
systems. The unsubstituted pyrazine was formed more with
olive oil, less with canola oil, and even less with sunflower
oil, whereas 2-methylpyrazine, 2,5-dimethylpyrazine, and
2,3-dimethylpyrazine were formed less with olive oil, more with
canola oil, and even more with sunflower.
Furthermore, although Blouin et al. (1981) did not assess
lipid oxidation during biscuit preparation, they found that the
presence of flavonoids, which exhibit significant antioxidant ac-
tivities (Miyake and Shibamoto, 1997), played a role in the pro-
duction of color in baked products prepared with wheat and
cottonseed flours. Thus, biscuits containing the extracted cot-
tonseed flours (free of flavonoids) were brown, and those to
which the flavonoid mixtures were added were yellow.
Existence of Common Intermediates in Both Lipid Oxidation
and Maillard Reaction Pathways
Although chemical structures of lipids and carbohydrates are
quite different, both lipid oxidation and Maillard reaction path-
ways produce carbonyl compounds, some of which are identical
when starting from both lipids and carbohydrates. Thus, for ex-
ample, two dicarbonyl compounds, namely glyoxal and methyl-
glyoxal, have been shown to be produced from both oxidized
lipids and carbohydrates. The formation of these dialdehydes
from carbohydrates and Amadori products has been described in
diverse studies. Hayashi and Namiki (1980) isolated and identi-
fied glyoxal dicyclohexylimine from a glucose/cyclohexylamine
model system. They proposed the cleavage of the sugar moi-
ety of the Schiff base at the initial stage of the amino-carbonyl
reaction, before the Amadori rearrangement, followed by for-
mation of a free radical and C2 products. Analogously, Hayashi
et al. (1986) identified methylglyoxal dialkylimine formation at
an early stage of the browning reaction of carbohydrates with
amines and amino acids, suggesting that this compound was
produced directly from the Amadori product. The production of
these two C2 and C3 sugar fragments in a glucose–β-alanine sys-
tem was negligible in acidic conditions, but increased with pH
in a manner parallel to the increase in browning and also to the
nitrogen/carbon ratio of the melanoidins (Hayashi and Namiki,
1986). In addition, Wolff et al. (1991) proposed the formation
of glyoxal as a consequence of autoxidation of glucose to form
this and other active intermediates.
Glyoxal and methyl glyoxal also have been shown to be lipid
oxidation products. Thus, they were found to be produced during
methyl linoleate autoxidation by Cobn and Day (1965), and these
data were later corroborated by diverse studies that reported gly-
oxal formation during UV irradiation of polyunsaturated fatty
acids (Niyati-Shirkhodsee and Shibamoto, 1993), during the ox-
idation of linoleic acid in an iron ascorbate model system (Loidl-
Stahlhofen and Spiteller, 1994; Mlakar and Spiteller, 1994), and
in autoxidizing arachidonic acid incubations (Fu et al., 1996).
These dialdehydes are believed to be produced by further oxi-
dation of α,β-unsaturated aldehydes produced during the lipid
peroxidation process (Mlakar and Spiteller, 1994).
In addition to carbonyl compounds, many other compounds
also have been shown to be produced in the browning produced
by both oxidized lipids and carbohydrates. These compounds
include diverse volatile (Zamora et al., 1994) and nonvolatile
heterocycles (Hidalgo et al., 1999). Among these compounds,
the formation of N -substituted hydroxyalkylpyrroles has a spe-
cial interest because of its implication in nonenzymatic browning
produced by both oxidized lipids and carbohydrates.
N -Substituted hydroxyalkylpyrroles were first described by
Hidalgo and Zamora (1993b) when they studied the reaction be-
tween the lipid oxidation product 4,5(E)-epoxy-2(E)-heptenal
 LIPID OXIDATION AND MAILLARD REACTION TO FOOD BROWNING
and butylamine and glycine methyl ester. 4,5-Epoxy-2-alkenals
are tertiary products of the lipid peroxidation. They are pro-
duced in the decomposition of intermediate epoxyhydroperoxy
fatty acids by a mechanism, depicted schematically in Figure 3,
which seems to be common for the different polyunsaturated
fatty acids. Thus, when starting from n-6 polyunsaturated fatty
acids, the epoxyalkenal that is obtained is 4,5(E)-epoxy-2(E)-
decenal by decomposition of an intermediate 12,13(E)-epoxy-9-
hydroperoxy-10-octadecenoic acid (Gardner and Selke, 1984).
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Analogously, the 4,5(E)-epoxy-2(E)-heptenal is the product of
oxidation of the n–3 polyunsaturated fatty acids (Frankel et al.,
1981). These epoxyalkenals, which are supposed to be interme-
diates in the formation of 4,5-dihydroxydecenal by peroxidation
of liver microsomal lipids (Benedetti et al., 1984), have been
detected in many different systems (Grosch, 1993). This mech-
anism is also valid for the formation of long chain fatty acids
with analogous 4,5-epoxy-1-oxo-2-pentene structure (Hidalgo
and Zamora, 1995b).
In the first step, the reaction between 4,5-epoxy-2-alkenals
and lysine amino groups produces two types of pyrrole deriva-
tives N -substituted pyrroles and N -substituted hydroxyalkylpy-
rroles (Zamora and Hidalgo, 1994) (Figure 3). N -Substituted
pyrroles are relatively stable, can be determined (Zamora et al.,
1995), and have been found in more than 20 fresh food prod-
ucts, including meats, fishes, vegetables, and nuts (Zamora et al.,
1999). However, N -substituted hydroxyalkylpyrroles polymer-
ize spontaneously, producing melanoidin-like polymers (see be-
low).
Analogous N -substituted hydroxyalkylpyrroles were also
produced from Maillard reactions. Wondrak et al. (1997) found
that 2-deoxy-D-ribose, in spite of the absence of an α-hydroxy
group that blocks enaminol formation and Amadori rearrange-
ment, exhibited a remarkable browning activity that may be,
in part, attributed to the formation of these N -substituted hy-
droxyalkylpyrroles. Thus, they isolated and characterized an
N -substituted 2-(hydroxymethyl)pyrrole derivative in the re-
action of 2-deoxy-D-ribose and methyl 4-aminobutyrate. This
compound was stabilized by the formation of a pyrrolidone
ring system with the methyl 4-aminobutyrate and was not de-
tectable in absence of this specific amino acid. The N -substituted
2-(hydroxymethyl)pyrrole was produced by 2,3-dehydration,
followed by vinylogous Amadori rearrangement and sub-
sequent cyclization (Figure 4). Analogously to the above de-
scribed N -substituted hydroxyalkylpyrroles, these compounds
displayed an unique polymerizing activity under mild conditions
and readily underwent polymerization to methylene-bridged
polypyrroles (see below).
Existence of Common Polymerization Mechanisms in Both
Lipid Oxidation and Maillard Reaction Pathways
The characterization of polymerization mechanisms in these
reactions is not easy, because the polymers are usually produced
by reaction of the most reactive intermediates, which are also the
53
compounds most difficulty isolated and characterized. There are
currently two main proposals for the mechanisms contributing
to melanoidin formation from both oxidized lipids and carbohy-
drates: aldol-type condensation and pyrrole polymerization.
The first mechanism described for nonenzymatic browning,
as a consequence of lipid oxidation, was a repeated aldol con-
densation. Since Mohammad et al. (1949) discovered that ac-
etaldehyde caused protein browning; it has been theorized that
Schiff base adducts lead to brown pigments. According to this,
the carbonyl compounds derived from unsaturated lipids read-
ily condense with protein-free amino groups to produce imino
Schiff bases. Then, Schiff bases polymerize by aldol conden-
sation, producing dimers and complex high-molecular weight
brown macromolecules. These polymeric brown materials are
unstable and generate new volatiles by scission of the macro-
molecule or dehydration, which affect the flavor characteristics
of foods during cooking and processing. In addition, the amino
compound even may cleave from the polymer, which may be
one of the reasons for the broad range of nitrogen content ob-
served in the polymer (Belitz and Grosch, 1999; Gardner, 1979;
Montgomery and Day, 1965).
An analogous mechanism has been suggested for melanoidin
formation in Maillard reactions. In this case, the melanoidin
skeleton is mainly built-up of sugar degradation products,
formed in the early stages of a Maillard reaction, polymerized
through aldol-type condensation, and possibly linked by amino
compounds (Cämmerer et al., 2002; Yaylayan and Kaminsky,
1998). In model melanoidins, the C-2 atom of amino acid is com-
monly incorporated into the polymer as an enamin-C (Hayase
et al., 1986). Kato and Tsuchida (1981) suggested a regular
composition of repeating units in melanoidins, but, in order to
explain the variations of the carbon/nitrogen ratio observed in
model melanoidins when using different reaction conditions,
Cämmerer and Kroh (1995) suggested a more flexible structure.
Thus, they proposed a structure that allows an easy insertion of
enamines of 1-amino-1-deoxyosuloses or decomposition prod-
ucts of diaminoketosyl- and diketosylamino compounds (Kroh
and Westphal, 1983). In addition, and because many reactive
centers are present in the main chain and also in the side chain,
the formation of furan bodies or N -heterocyclics, such as pyrro-
laldehyde (Kato and Tsuchida, 1981), can be explained by in-
tramolecular cyclisation. Furthermore, decarboxylations and the
elimination of water are also possible.
An additional mechanism for the formation of nonenzymatic
brown polymers was proposed more recently. It was described
for the browning developed with some lipid oxidation products,
and it is based on the polymerization of the N -substituted hy-
droxyalkylpyrroles. These compounds polymerize spontaneou-
sly; dimers, trimers, tetramers, and higher polymers were
characterized by different techniques, which included nuclear
magnetic resonance spectroscopy, mass spectrometry, and gel
filtration chromatography (Hidalgo and Zamora, 1993b). The
route of formation of these polymers is given in Figure 3.
Analogous macromolecular polypyrrolic structures were
found by Tressl et al. (1998b); when incubated under mild
 54 R. ZAMORA AND F. J. HIDALGO
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Figure 3 Formation and polymerization of N -substituted hydroxyalkylpyrroles in the lipid oxidation pathway.
 LIPID OXIDATION AND MAILLARD REACTION TO FOOD BROWNING 55
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Figure 4 Formation and polymerization of N -substituted hydroxyalkylpyrroles in the Maillard reaction pathway.

conditions, the N -methyl-1-hydroxymethylpyrrole originated
from the Maillard reaction of methylamine with 2-deoxy-D-
ribose. Repetitive electrophilic substitution and subsequent de-
formilation and dehydration/dehydrogenation lead to the for-
mation of linear methylene-bridge polypyrroles within minutes
(Figure 4), analogously to the porphyrinogen biosynthesis from
porphobilinogen, a 2-aminomethyl substituted pyrrole. N -
Substitution inhibited the cyclation of the tetramer, and linear
species of up to 12 pyrrole units were generated. Starting from
the hexamer, subsequent dehydrogenation with formation of up
to four conjugated pyrroles was observed.
The formation of these polypyrrolic polymers from either
oxidized lipids or carbohydrates, which may be followed spec-
trophotometrically (Hidalgo et al., 1998; Zamora et al., 2000),
gave a satisfactory explanation for the color and fluorescence
produced in these reactions (Hidalgo and Zamora, 1993b, 1995a;
Hidalgo et al., 1999; Zamora and Hidalgo, 1992, 1995a), as
well as the formation of short chain aldehydes and volatile
heterocyclic compounds (Zamora and Hidalgo, 1995b; Zamora
et al., 1994). However, it does not explain some findings of
melanoidins with a low nitrogen content. It might be a conse-
quence of either the difficulty of purifying melanoidins, which
may be contaminated by low molecular weight monomers or by
other polymers produced exclusively by polymerization of un-
saturated fatty acids or carbohydrates, or that the melanoidins are
not a homogeneous polymer, but a mixture of different polymers
produced by different mechanisms. According to our present
knowledge, both possibilities are likely occurring.
 56 R. ZAMORA AND F. J. HIDALGO
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Figure 5 Known interactions between Maillard reaction and lipid oxidation pathways in nonenzymatic browning development.
Similarities between Oxidized Lipid- and Maillard-Modified
Proteins
If lipid oxidation and Maillard reaction pathways follow par-
allel mechanisms, the differences between the products of one
or other pathways should be very small, at least from a nonen-
zymatic browning point of view.
Although there is a lack of studies in this sense, Hidalgo
et al. (1999) studied the incubation of bovine serum albumin in
the presence of ribose, methyl linoleate hydroperoxides, and the
secondary products of methyl linoleate oxidation at five temper-
atures ranging from 25◦ C to 120◦ C. They found that all treated
proteins exhibited similar colors and fluorescence spectra; the
spectra of their Ehrlich adducts were also analogous. The only
difference observed among the treated proteins was that at 25–
50◦ C the proteins treated with oxidized lipids exhibited higher
color changes, amino acid losses, and pyrrolization than the
bovine serum albumin treated with ribose. These effects were
much higher in proteins treated with ribose at 80–120◦ C. In
addition, all proteins modified by both oxidized lipids and car-
bohydrates exhibited an analogous antioxidant activity that was
correlated to the amino acid losses produced during the nonen-
zymatic browning (Alaiz et al., 1997b; Alaiz et al., 1999).
All these results are in agreement with a similarity for brown-
ed proteins obtained from both oxidized lipids and carbohy-
drates. In addition, both reactions seem to be complementary,
because melanoidin formation derived from oxidized lipids can
be produced under conditions different for those melanoidins
produced from carbohydrate/protein reactions.
CONCLUSION
The above results show that lipid oxidation products are not
only influencing Maillard pathway and vice versa, but both path-
ways have common intermediates and polymerization mecha-
nisms and seem to produce similar products, at least from a
nonenzymatic browning point of view. Therefore, both reactions
are so interrelated that they should be considered simultaneously
to understand the products of the Maillard reaction in the pres-
ence of lipids and vice versa. All these conclusions have been
summarized in Figure 5. According to the above results, and in
relation to melanoidin formation, lipid oxidation and Maillard
reaction should be included in one general pathway that can be
initiated by both lipids and carbohydrates. This general mech-
anism should likely be completed with the other reactions that
also produce nonenzymatic browning and might also influence
lipid oxidation and Maillard pathways.
ACKNOWLEDGMENTS
This study was supported in part by the Ministerio de Ciencia
y Tecnologı́a of Spain (Project AGL2003-02280) and the Junta
de Andalucı́a (Project AGR 0135).
 LIPID OXIDATION AND MAILLARD REACTION TO FOOD BROWNING
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