The Role of Oxygen in Lipid Oxidation Reactions - A Review

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The Role of Oxygen in Lipid

Oxidation Reactions: A Review
David R. Johnson1 and Eric A. Decker1,2
1
Chenoweth Laboratory, Department of Food Science, University of Massachusetts, Amherst,
Massachusetts 01003; email: [email protected]
2
Bioactive Natural Products Research Group, Department of Biochemistry, King Abdulaziz
University, Jeddah 21589, Saudi Arabia
Annu. Rev. Food Sci. Technol. 2015. 6:17190
Keywords
First published online as a Review in Advance on

February 2, 2015
lipid oxidation, dissolved oxygen, headspace oxygen, oxygen scavenging,

antioxidant solutions
The Annual Review of Food Science and Technology is

online at food.annualreviews.org
This articles doi:
10.1146/annurev-food-022814-015532
c 2015 by Annual Reviews.
Copyright
All rights reserved
Abstract
The susceptibility of food oil to quality loss is largely determined by the presence of oxygen. This article reviews the current understanding concerning
the effect of oxygen types, location, and concentration on the oxidative stability of foods. It also discusses the major factors that inuence the interaction
between oxygen and lipids such as antioxidants, prooxidants, reactive oxygen
species (ROS), environmental conditions, and oxygen scavengers. Research
has shown that the amount of oxygen needed to cause oxidation is generally very small and that by reducing oxygen concentration in containers to
less than 2%, oxidative stability can be greatly enhanced. However, very few
studies have systematically examined the oxygen levels needed to reduce, or
inhibit, lipid oxidation processes. Thus, a more comprehensive understanding of the relationship between oxygen levels and lipid oxidation is necessary
for the development of innovative antioxidant solutions and package designs
that prolong the quality of foods containing lipids.
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INTRODUCTION

Lipid oxidation is the principal deteriorative reaction during food processing and storage that limits
shelf life of most microbiologically stable foods (Andersson & Lingnert 1997). The oxidation of
food products not only sharply curtails shelf life, but can also pose hazards to human health. The
generation of toxic reaction by-products and the destruction of essential vitamins during oxidation
are responsible for negatively impacting the safety and wholesomeness of foods (Kubow 1992).
In general, the oxidative susceptibility of food products is increasing because of food industry
trends to remove hydrogenated oils, use bioactive unsaturated fatty acids, and replace potent
synthetic antioxidants with ones of natural origin. Specically, the incorporation of unsaturated
fatty acids presents a difcult challenge in foods because unsaturated fatty acids are prone to
deleterious chemical reactions with oxygen. Oxygen, a diatomic gaseous molecule ubiquitously
present in the atmosphere, is free to interact with reactive unsaturated fatty acids and is ultimately
responsible for quality deterioration of lipids (McClements & Decker 2000). Two forms of oxygen
are responsible for the different chemical mechanisms involved in the oxidation of edible oils. The
more reactive form, singlet oxygen (1 O2 ), can quickly promote lipid oxidation in foods containing
photosensitizers. The more common form, triplet oxygen (3 O2 ), is responsible for the free radical
chain reaction of lipid oxidation. Both oxidative pathways produce undesirable low molecular
weight volatiles that have human sensory threshold values as low as 0.01 ppb, as seen in sh oils
(Hsieh & Kinsella 1989). Extremely low sensory thresholds of lipid oxidation products demand
the prevention of even minimal lipid degradation. As a result, efforts made to inhibit oxidative
reactions in food products should aim to extend the lag time prior to generation of volatile lipid
oxidation products.
Antioxidant supplementation is a common strategy for avoiding oxidative reactions in the
processing and storage of food. Historically, antioxidants have been used in food systems to
prevent or mediate oxidative damage by scavenging free radicals before the propagation phase
of lipid oxidation (Ahn et al. 1993). However, an industry trend to replace powerful synthetic
antioxidants with natural compounds has recently emerged, and these natural antioxidants have
proven to be a less effective solution to limit oxidation. Now, innovative solutions are needed to
maintain the oxidative stability of edible oils. Because oxygen is essential for the degradation of
lipids, a more complete understanding of oxygens role and reactivity in lipid-containing systems
will lead to a successful design of alternative, effective antioxidative solutions.
Lipid Oxidation: Mechanism

The classical scheme of lipid oxidation involves three stages: initiation, propagation, and termination (Scheme 1). Deterioration of fatty acids is initiated when a hydrogen atom is abstracted
from a fatty acid, forming an alkyl radical (L ). Free radicals on unsaturated fatty acids can
form via hydrogen abstraction mechanisms from initiating free radicals (e.g., hydroxyl radicals)
present in foods. Hydrogen abstraction depends on the bond dissociation energy of the covalent
Initiation:
LH L + H
Scheme 1
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Propagation:
L + 3O2 LOO
LOO + LH LOOH + L
Termination:
LOO + L LOOL
L + L LL
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Table 1 Bond dissociation energy for carbon-hydrogen covalent bond on fatty acids (McClements
& Decker 2008)

Carbon-hydrogen covalent bond
Bond dissociation energy (kcal/mol)
Saturated (aliphatic chain)
98
Monounsaturated (adjacent to double bond)
89
Polyunsaturated (methylene-interrupted carbon)
80
carbon-hydrogen bond, which is weakened by adjacent electron-rich double bonds in unsaturated

fatty acids. Polyunsaturated fatty acids (PUFAs) are particularly susceptible to hydrogen abstraction due to the presence of single or multiple methylene-interrupted hydrogens with lower bond
dissociation energies (Table 1). After alkyl radical formation, electrons of the double bond stabilize the free radical through delocalization over a conjugated diene structure converting one of the
double bonds to the more stable trans form. Once a lipid radical has formed, triplet oxygen (3 O2 )
reacts quickly with the alkyl radical at a rate of 28 109 M1 s1 under normal oxygen pressure to
form a covalent bond with the lipid (Zhu & Sevilla 1990). The resulting peroxyl radical (LOO ) is
able to abstract another hydrogen from an unsaturated lipid to form hydroperoxides (LOOH) and
propagate the free radical chain reaction by producing another free radical on the second fatty acid.
Notably, lipid hydroperoxides do not cause rancidity. Rather, lipid hydroperoxides can be broken
down by -scission reactions (triggered by light, heat, or transition metals) into aldehydes, ketones,
acids, esters, and alcohols that are associated with off-avors. Eventually, two radicals may react to
form a nonradical species that terminates the radical chain reaction. The damage caused by oxygen
incorporation has been studied over the past 60 years (Frankel 2005, Labuza 1971); however, it
remains unclear how to limit its reactivity in different foods. Therefore, this review focuses on the
role of oxygen in lipid reactions and available strategies to enhance the oxidative stability of foods.
FACTORS THAT INFLUENCE LIPID OXIDATION

Lipid Composition
Foods exist as complex chemical systems. There are numerous elements within and surrounding
foods that can often interact in various ways with one another to either promote or inhibit lipid
oxidation, a phenomenon that highlights the difculty in isolating a single cause of deterioration.
Lipid composition, minor components of the lipid and aqueous phases, and food environment
are some of the major factors determining the oxidative susceptibility of lipids. The chemical
structure of the lipid substrate largely determines the oxidative stability of foods. Lipids that
possess higher degrees of unsaturated double bonds are more prone to oxidation. For example,
the relative oxidation rates for fatty acids containing 18 carbons (18:1, 18:2, 18:3) that differ only
in the number of double bonds is 1, 12, 25, respectively (Holman & Elmer 1947). As previously
mentioned, the presence of double bonds lowers the energy needed to abstract allylic hydrogens
and enhances the rate of lipid radical chain reactions. Until recently, unsaturated lipids were
commonly catalytically hydrogenated to remove double bonds and increase oxidative stability.
However, insights into the health benets of PUFAs and the negative effects of trans fatty acids
derived from the hydrogenation process have since left food scientists searching for novel ways to
incorporate and protect unsaturated fatty acids in food products.
Minor Components
Minor components within the food system interact in a complex balance between antioxidant
and prooxidant factors. Minor components that function as antioxidants inhibit or slow oxidative
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processes. The inhibition of the lipid free radical chain reaction during oxidation is of practical
importance because it can limit the extent of degradation of unsaturated fatty acids. Antioxidants
inhibit oxidation in foods by inactivating free radicals, quenching oxygen and photosensitizers,
and chelating prooxidative metal ions (Choe & Min 2009). Tocopherols, carotenoids, ascorbic
acid, and phenolics are major antioxidant components commonly found in foods (Frankel 2005).
Yet, antioxidant activity is highly dependent on the concentration and location of the antioxidant
within foods. In some cases, the same antioxidant that inhibits oxidation in one food system may
impart a prooxidative effect in another. For instance, ascorbic acid (1,161 M) added to a bulk
stripped corn oil was shown to exhibit antioxidant activity by inhibiting the formation of the
secondary lipid oxidation product, hexanal (Frankel et al. 1994). However, ascorbic acid added at
a low concentration (50 M) to an oil-in-water emulsion system resulted in a prooxidant effect
(Alamed et al. 2009). One explanation for this phenomenon is that in the bulk oil system high
levels of ascorbic acid concentrate at the oil-water interfaces and limit oxidation by free radical
scavenging activity. On the contrary, at lower concentrations, in oil-in-water emulsions, ascorbic
acid is dispersed throughout the matrix, and its free radical scavenging activity is outweighed by its
strong reduction potential, which redox cycles transition metals to their more active prooxidative
state (Alamed et al. 2009, Decker & Hultin 1992). Alternatively, ascorbic acid might not be
prooxidative in bulk oils because iron is not a major prooxidant. Clearly, the overall antioxidantprooxidant balance regarding location and concentration is important to consider when minor
components are supplemented in foods.
Although antioxidant components contribute to inherent oxidative stability of edible oils, foods
are constantly exposed to prooxidants that threaten to destabilize oxidative stability. Transition
metals, such as iron and copper, are minor components found in foods that can serve to both
initiate and accelerate lipid oxidation. Oxidation can be initiated by transition metals through
electron transfer reactions with 3 O2 and lipids that produce reactive oxygen species (ROS) or alkyl
radicals, respectively (Scheme 2). Iron and copper can accelerate oxidation when they undergo
redox cycling to decompose hydroperoxides into reactive lipid radicals, as shown in Scheme 2.
Although copper is more reactive at promoting lipid breakdown, iron is much more abundant
in both aqueous and oil environments. Iron was found in tap water at 200 g L1 , whereas
copper was at 20 g L1 , and iron concentrations were at levels 1001,000 times higher than
copper in bulk olive and soybean oils (Choe & Min 2006, Hu et al. 2002). Importantly, iron is
still a contaminant in bulk oils after rening at levels high enough (0.20 ppm iron in soybean
oil) to cause signicant oxidative instability (Sleeter 1981). Additionally, many foods are fortied
with iron to supplement health; thus, its inclusion in foods contributes to potential prooxidative
effects. Mancuso et al. (1999) clearly demonstrated the prooxidant effects of iron in oil-in-water
emulsions when addition of apo-transferrin, a highly iron-specic binding transport protein, nearly
resulted in complete inhibition of lipid oxidation in Tween 20stabilized salmon oil-in-water

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Fe2+ + 3O2 Fe3+ + O2

Fe3+ + LH Fe2+ + L + H+
Fe2+ + H2O2 Fe3+ + OH + HO
LOOH + Fe2+ (or Cu+) LO + Fe3+ (or Cu2+) + HO
LOOH + Fe3+ (or Cu2+) LOO + Fe2+ (or Cu+) + H+
Scheme 2
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emulsions. As with other transition metals, iron can exist in multiple chemical oxidation states.
The ferrous (Fe+2 ) state is an order of magnitude more reactive at catalyzing LOOH breakdown
than the ferric state (Fe+3 ) (Choe & Min 2006). Thus, reducing compounds found in foods can
promote lipid oxidation by redox cycling transition metals to their more reactive state. The effect
of irons oxidation state can be observed from oxygen consumption data in a liposome system
following addition of ferrous iron. Consumption of oxygen, following addition of Fe+2 , increased
exponentially as ferrous iron promotes the generation of fatty acid radicals that allow oxygen to
form peroxyl radicals (Mozuraityte et al. 2008). Kristinova et al. (2014) showed that one ferrous
molecule could promote the consumption of ve oxygen molecules via lipid oxidation reactions
in a herring oil emulsion system.
Temperature
Environmental factors, such as temperature, can either increase or decrease lipid oxidation rates
depending on the system. For instance, in most foods a 10 C increase in temperature corresponds
to approximately a doubling in the rate of oxidation (Matthaus 2010). Elevated temperatures can
increase lipid oxidation rates by promoting hydroperoxide breakdown in a process that generates
free radicals. Accordingly, an effective way to control lipid oxidation is to decrease the storage
temperature of the oil. Lowering the storage temperature of sh oil from +4 C to 18 C showed
a decrease in both primary and secondary lipid oxidation products, nearly doubling the shelf life of
the sh oil (Boran et al. 2006). Unfortunately, low-temperature storage is not suitable for all foods.
For example, low temperatures can cause solidication of the oil resulting in changes in appearance
(cloudiness), inability to pour, and disruption of oil-in-water emulsions (McClements & Decker
2008). In general, high temperatures will increase free radical formation, but this may not result
in immediate alterations in food quality because most foods contain inherent antioxidants that
provide a natural resistance to oxidation. Therefore, the impact of high-temperature processing
is not affected by temperature alone, but also the duration of time that temperature is applied.
Broncano et al. (2009) demonstrated during meat roasting that heating for a longer time at a lower
temperature caused a higher increase in secondary lipid oxidation products compared to heating
at a higher temperature for a shorter time. Other studies (Rastogi et al. 2006, Santos et al. 2013)
support the nding that lipid oxidation during cooking processes may be more affected by longer
cooking times and lower temperatures than higher temperatures and shorter cooking times. There
exist instances when an extreme increase in temperature actually decreases the development of
oxidative rancidity, such as in heated frying oils that are not being actively used to cook foods. In
this situation, elevated temperatures decrease oxygen levels so that oxygen is not available for the
formation of hydroperoxides, and the oxidation process results in termination reactions between
alkyl radicals (Matthaus 2010). This reaction yields fatty acid polymers that do not impact avor,
unlike volatiles derived from hydroperoxide decomposition (Choe & Min 2007). The oxidative
stability resulting from decreased amounts of oxygen in unused, heated frying oil shows that
molecular oxygen is ultimately responsible for the deterioration of edible oils. The effects of
oxygen in lipid oxidation reactions are discussed further in subsequent sections.
OXYGEN SPECIES
Triplet Oxygen
An important step in lipid oxidation occurs when atmospheric triplet oxygen (3 O2 ) reacts with a
fatty acid radical. The chemical reactivity of triplet oxygen with fatty acid radicals is more easily
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or
Energy
1O
Singlet oxygen (1O2)

HOOC
Triplet oxygen (3O2)
Figure 1
Molecular orbitals of singlet and triplet oxygen. Singlet oxygen addition to linoleic acids electron-rich double bonds in photosensitized
oxidation (redrawn from McClements & Decker 2008).
understood when the state of oxygens electron molecular orbitals is considered (Figure 1). Abiding by Hunds Rule, oxygen most commonly exists as a biradical in its ground state (3 O2 ) that results
in two unpaired electrons with parallel spins (Halliwell & Gutteridge 1990). The nomenclature for
the so-called triplet and singlet electronic states is derived from the molecules spin multiplicity,
dened as 2S+1, where S is the total spin number. Depending on the angular direction of the
electronic spin, the S value can be either +1/2 or 1/2. If oxygens two unpaired electrons have
parallel spins, then the spin multiplicity will be 2(1/2 + 1/2) + 1 = 3, or simply, in the triplet state.
Electrons that have antiparallel spin values within the same orbital will cancel each other out, which
results in the singlet state. Because the electronic conguration of unsaturated fatty acids exists in
the singlet state, its reaction with triplet oxygen would result in an unlikely highly endothermic
reaction and is thus an improbable occurrence (Korycka-Dahl & Richardson 1978). Therefore,
oxidation of edible oils rst requires the formation of a free radical to overcome electronic spin
restrictions and make the reaction between oxygen and the fatty acid thermodynamically favorable.
Reactive Oxygen Species

Reactivity of triplet oxygen with unsaturated fats is forbidden because of spin restrictions, but
spin restrictions can be overcome by the generation of ROS (Hsieh & Kinsella 1989). ROS are
formed when oxygen is reduced during oxidation of other molecules. Hydroxyl (HO ), peroxyl
(ROO ), alkoxyl (RO ), and hydroperoxyl (HOO ) radicals, as well as the superoxide anion (O2 ),
are ROS that can accelerate lipid oxidation in foods (Choe & Min 2005). Hydroxyl radicals are
ROS primarily formed from degradation of H2 O2 by UV light and metals (Gutteridge 1995).
Hydroxyl radicals are important initiators in lipid oxidation, abstracting hydrogen from a lipid
and creating a carbon-centered radical on the alkyl chain. As previously discussed, peroxyl and
alkoxyl radicals function as intermediates in the propagation phase of lipid oxidation. The highenergy peroxyl and alkoxyl radicals can abstract hydrogens from neighboring lipids, or in the case
of alkoxyl radicals can break the aliphatic chain of a fatty acid.
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Other ROS in foods indirectly inuence lipid oxidation through enhancement of prooxidant
activity or as precursors to free radicals. The superoxide anion is the result of a one-electron
reduction of triplet oxygen forming a radical anion (O2 ). The superoxide anion can be produced in
foods enzymatically (xanthine oxidase and nicotinamide adenine dinucleotide phosphate oxidase),
by photoactivation of tetrapyrroles (e.g., hemoglobin and chlorophyll), or by irradiation that
allows hydrated electrons to reduce triplet oxygen (Choe & Min 2005). The superoxide anion
itself is not an initiator of free radical lipid oxidation because its reduction potential is too low
to abstract hydrogen from unsaturated fatty acids (Bielski et al. 1983). However, the superoxide
anion can reduce transition metals to a more active state, thus promoting lipid oxidation. The
superoxide anion can also become protonated at low pH to form hydroperoxy radicals that carry
a reduction potential capable of abstracting hydrogen from unsaturated fatty acids. To limit the
initiating and propagating effect of the superoxide anion, almost all biological tissues contain
superoxide dismutase, which converts the superoxide anion into triplet oxygen and hydrogen
peroxide (McClements & Decker 2008).
Singlet Oxygen
Photosensitized oxidation differs from oxidation by triplet oxygen because it can produce highenergy oxygen species that abstract hydrogen atoms from unsaturated fatty acids, or ROS, without
formation of a carbon-based free radical (Figure 1). Photosensitizers such as chlorophyll, avins
(e.g., riboavin), and myoglobin absorb light in the visible or near-UV region and become electronically excited (Frankel 2005). Depending on the concentration of oxygen, the electronically
excited sensitizer can cause photosensitized oxidation by two distinct mechanisms. Under lower
oxygen concentrations, type I mechanisms proceed with the photosensitizer possessing enough
energy to independently abstract a hydrogen atom from a fatty acid generating a free radical. Reaction products of type I mechanisms are consistent with those of nonsinglet oxygenpromoted
oxidation, and the photosensitizer acts as a free radical generator (Min & Boff 2002). Type II
reactions occur when oxygen is readily available and involve the transfer of energy from the photosensitizer to oxygen. Energy transfer to oxygen causes the spin of 2p orbital electrons to shift
into opposing directions, thereby generating singlet oxygen (1 O2 ).
Singlet oxygen may exist in one of ve congurations with the 1 conguration, indicating
two antiparallel electrons existing in one orbital, which is the most common in food (Choe &
Min 2006). The higher electronic state of singlet oxygen creates an energy difference of 22.5 kcal
above the triplet state of oxygen (Korycka-Dahl & Richardson 1978). Singlet oxygens electron
conguration allows it to directly attack the electron-rich double bonds of unsaturated lipids, at
a rate 1,500 times greater than triplet oxygen (Garca-Torres et al. 2009). Andersson & Lingnert
(1998) demonstrated the inuence of photosensitized oxidation when hexanal, a secondary lipid
oxidation product, was produced at concentrations 330 times higher in spray-dried cream stored
in uorescent light compared to a control stored in the dark. In this case, the photosensitizer,
riboavin, present in the cream powder was capable of generating singlet oxygen that enhanced
the rate of oxidation. Researchers can detect the presence of singlet oxygen because of its ability to
react with the carbons at either end of the unsaturated fatty acid double bond, forming unique lipid
oxidation hydroperoxides. For example, in a linoleate system singlet oxygen has the potential to
generate four lipid hydroperoxides (conjugated and non-conjugated) compared to the typical two
(conjugated double bond conguration) formed in traditional oxidation (Table 2) (Frankel 2005,
Rawls & Van Santen 1970). Rawls & Van Santen (1970) reported that photosensitized oxidation
is temperature independent as a result of the low activation energy (0 to 6 kcal/mol) required for
singlet oxidation of edible oils (Choe & Min 2006). Thus, at lower temperatures singlet oxygen
threatens oxidative stability because of its potential to initiate lipid oxidation reactions.
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Table 2 Hydroperoxides formed from oxidation of linoleate by singlet and triplet oxygen (modified
from Min & Boff 2002)
Lipid hydroperoxides from linoleate
Oxygen type
Conjugated
Nonconjugated
Singlet oxygen
9-OOH
13-OOH
10-OOH
12-OOH
Triplet oxygen
9-OOH
13-OOH
Minimal

Given singlet oxygens potential to initiate lipid oxidation, control measures are needed to
protect foods. Besides packaging that excludes light, singlet oxygen quenchers are the most effective
means of preventing photosensitized oxidation. Quenchers function by either physical or chemical
mechanisms to inactivate singlet oxygen. Physical quenching returns singlet oxygen, or an excited
photosensitizer, to its ground state without generating oxidized products or consuming oxygen
(Min & Boff 2002). Carotenoids are a diverse group of yellow to red colored singlet oxygen
quenchers (e.g., -carotene, lycopene, and lutein) that physically inactivate 1 O2 by absorbing
energy over nine or more conjugated double bonds. The absorption produces an excited-state
carotenoid that vibrates to transfer the absorbed energy to the surrounding system giving off
heat. Lee & Min (1990) found that carotenoids could protect against photosensitized oxidation
in soybean oil and that antioxidant effectiveness increased with the number of conjugated double
bonds. -Carotene is the most common carotenoid in foods and one of the most potent singlet
oxygen quenchers, with 1 mol inactivating between 250 and 1,000 molecules of singlet oxygen
(Foote et al. 1970). Tocopherols are another class of singlet oxygen quenchers that physically
convert singlet oxygen to triplet oxygen by charge transfer and electron donation (Kamal-Eldin
& Appelqvist 1996). Carotenoids and tocopherols, as well as ascorbic acid, can also chemically
quench singlet oxygen, which involves singlet oxygen attacking the double bond of the antioxidant.
However, chemical quenching consumes both oxygen and the quencher to generate an oxidized
antioxidant. For carotenoids, protection by physical quenching is preferred because chemical
inactivation of singlet oxygen rapidly degrades color (Min & Boff 2002).
OXYGEN IN FOODS CONTAINING LIPIDS

Oxygen Location
Oxygen is the primary reactant in lipid oxidation reactions that cause rancidity in foods. The most
abundant and stable form of oxygen, triplet oxygen, can be present as a dissolved gas within the
food matrix, as nondissolved gas in the headspace above the food, or as a nondissolved gas trapped
in solid or semisolid matrices (Figure 2) (e.g., whipped cream, mayonnaise, processed meats).
As a dissolved gas, the proximity and accessibility of dissolved oxygen to lipids reduce oxidative
stability. Specically, dissolved oxygen content has been correlated with oxygen disappearance,
generation of free radicals, and formation of volatile lipid oxidation products in food (Min & Wen
1983, Parenti et al. 2007). Dissolved oxygen concentration follows Henrys Law, meaning that at
equilibrium the solubility of oxygen is directly proportional to the partial pressure of the oxygen
above the food (Ke & Ackman 1973). In addition to pressure effects, the foods composition
inuences the level of dissolved oxygen. Oxygen is approximately 510 times more soluble in
bulk oil than pure water at 20 C, with saturation occurring at 55 ppm and 510 ppm oxygen,
respectively (Aho & Wahlroos 1967, Montgomery et al. 1964). In comparison to the same volume
of water, atmospheric air contains approximately 30 times more oxygen (Andersson 1998). The
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O2
O2
O2
O2
O2
Headspace
oxygen
O2
O2
O2
O2
O2
O2
O2
O2
O2
O2 crossing
packaging
barrier
O2
O2

O2
O2
O2
O2
Entrapped
oxygen
(e.g., foam)
O2
O2
O2
O2
O2
O2
Dissolved
oxygen
O2
O2
Figure 2
Schematic diagram of oxygens location in an enclosed food/beverage system.
solubility of oxygen in food is temperature dependent, with an increase in temperature driving

oxygen from the dissolved state into the headspace. However, at temperatures greater than 60 C,
dissolved oxygen concentrations decrease rapidly by both heat-accelerated oxidation reactions and
reduced oxygen solubility (Chen et al. 2011).
Headspace oxygen is the nondissolved gas present above the foodstuff. Although headspace
oxygen has less surface area contact with lipids than dissolved oxygen, it still poses a threat to
lipid oxidation as a reservoir of oxygen (Quast & Karel 1971). Oxygen can be transported from
the headspace and dissolved in the food by either diffusion or mechanical agitation (Andersson
1998). Oxygen diffusion into food is driven by a concentration differential between headspace and
dissolved oxygen. Assuming that a steady state has been reached between diffusion and oxygen
consumption (e.g., lipid oxidation reactions), the oxygen concentration in the oil can be expressed
as dd ct = VDSZ (c 0 c ) kc = 0, where c is the oxygen concentration, D is the diffusion coefcient, S
is the oil-oxygen interfacial area, V is the volume of the oil, Z is the thickness of the diffusion lm
in the oil, and k represents the rate constants of oxidative processes occurring in the induction
phase of lipid oxidation (Simon

et al. 2000). Moreover, the rate that oxygen can travel through
a medium, referred to as diffusivity, is quantied by diffusion coefcients. Davidson et al. (1952)
found that olive oil had an oxygen diffusion coefcient of 0.75 109 m2 s1 , whereas lards
rate of oxygen transfer was found to be 0.40 109 m2 s1 . Whether this difference was due to
the mediums viscosity or is the result of oxidative reactions interfering with the measurement is
difcult to determine. What is certain is that the food composition and environmental conditions
affect the location of oxygen and its ability to diffuse into a food.
The Effect on Oxygen Concentration

Reducing the amount of oxygen within foods has been widely regarded as an effective solution to
retard lipid oxidation (Chen et al. 2011, Choe & Min 2006, McClements & Decker 2000). The
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reaction between triplet oxygen and an alkyl radical proceeds at a very fast, diffusion-limited rate
with a rate constant of 109 M1 s1 at normal oxygen pressure. This reaction is fast because no
quantum mechanical, thermodynamic, or kinetic barriers exist between the unpaired electrons of
oxygen and the alkyl radical (Dunford 1987). Researchers hypothesize that at higher concentrations
of oxygen the oxidation rate is not limited by oxygen diffusion, but rather is dependent on the
lipid substrate and/or prooxidant concentrations (Labuza 1971, McClements & Decker 2008).
Evidence suggests that if the oxygen concentration is reduced signicantly, then the rate of lipid
oxidation could be limited. Unfortunately, there is a lack of comprehensive studies detailing the
effect of concentrations on the rate and extent of lipid oxidation.
Many different units have been used to describe the concentration of oxygen, but because most
authors express oxygen as a percentage of the total atmosphere this review uses the term percentage (%) to refer to oxygen concentration in the headspace, instead of oxygen partial pressure.
Headspace oxygen concentrations as a percentage describe the oxygen volume/volume concentration at 20 C and standard pressure (101.3 kPa), whereas dissolved oxygen is reported as ppm.
Marcuse & Fredriksson (1968) demonstrated that lowering the oxygen in the headspace above
linoleate from 2.0% to 1.0% decreased oxidation to a greater extent than a reduction from 21%
to 2.0%. Their study highlights that lower oxygen concentrations have a higher relative effect on
oxidation rates, likely because diffusion-limited reaction rates can only be decreased when oxygen
levels are very low. However, as discussed above, the composition and structure of foods determine
the likelihood of oxygen-lipid radical interactions. To highlight this, we discuss the relationship
between oxygen concentrations and lipid oxidation in different foods below.

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Bulk Oils
Oxygen in bulk oil systems, either present in the headspace or dissolved in the oil, is a primary
determinant of the extent of lipid oxidation. In frying oils, decreased headspace oxygen concentrations have also been shown to enhance stability. Decreasing the concentration of headspace
oxygen from 20% to 2% above high-oleic safower frying oil completely inhibited the formation
of carbonyls, a product of lipid oxidation, whereas 20% oxygen increased the carbonyls to greater
than 150 meq/kg oil after 30 h (Fujisaki et al. 2000). Additionally, the endogenous tocopherols
in the frying oil were completely lost at 20% headspace oxygen concentration, but no detectable
change in tocopherol concentration could be seen at 2.0% oxygen. Andersson & Lingnert (1999)
showed that in lipid oxidation of rapeseed oil, as measured by oxygen consumption and peroxide
value, headspace oxygen concentrations below 0.5% strongly inuenced the oxidation rate. The
increasing inuence of oxygen at low levels is also supported in studies of dissolved oxygen as well.
A study conducted by Min & Wen (1983) found that the rate of dissolved oxygen disappearance in
soybean oil was three times as fast at 8.5 ppm oxygen compared to that of soybean oil containing
2.5 ppm oxygen. Limiting the dissolved oxygen content is also important because it appears that
dissolved oxygen serves as a starter for oxidation in bulk extra virgin olive oil (Masella et al. 2010).
Levels of dissolved oxygen contents commonly found in bulk commercial oils are capable of generating hydroperoxides at a value of approximately 10 meq/kg oil (Przybylski & Eskin 1988). At
this peroxide level, the eventual breakdown into secondary reaction products would yield volatiles
that would render the food unacceptable to consumers.
Heterogeneous Lipid Systems

Heterogeneous food systems (e.g., muscle foods, emulsions, powders) are inherently more complex than bulk oil; however, the oxidative stability of these foods remains just as dependent on
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oxygen levels. OGrady et al. (2000) determined the effect of high-oxygen concentrations on lipid
oxidation in packaged minced beef by thiobarbituric acid reactive substances (TBARS). The researchers found that increasing oxygen concentration to 40%, 60%, and 80% total headspace did
not show a statistical difference in level of oxidation, whereas 20% oxygen showed lipid oxidation
to a lesser extent. The results from this study emphasize that at levels of oxygen greater than
atmospheric conditions, lipid oxidation is not limited by oxygen availability. In the case of muscle
foods, oxygen accessibility is also limited by diffusivity given that oxygen only penetrates 210 mm
into the food within 24 h and the rate slows as time progresses (Kilic & Cassens 1998). The oxygen diffusivity limitation explains, in part, why the non-minced packaged meat in OGrady et al.s
(2000) study experienced less oxidation across all levels of oxygen compared to the minced variety.
The processing of muscle foods produces an increase in surface area and disrupts cellular membranes, which permits an increase in the rate of oxygen diffusion to unsaturated lipids (Andreo
et al. 2003). In a similar manner, changes to the molecular environment of emulsied foods also
dictate oxidative stability. For instance, at low oxygen concentrations (i.e., below 2.0% oxygen),
oxidation reactions in a Tween 20stabilized oil-in-water emulsion were limited by oxygen diffusion through the aqueous phase (Marcuse & Fredriksson 1968, 1969). Not surprisingly, the shelf
life of powdered foods is likewise limited by oxygen concentrations. Andersson & Lingnert (1998)
showed that lowering the headspace oxygen level down to 0.03% above powdered cream greatly
reduced the formation of secondary lipid oxidation products compared to a control at atmospheric
conditions. However, the 0.03% oxygen level in the study was still not low enough to protect the
sample from the production of rancid off-avors as determined by sensory studies after 35 weeks.
Examinations that evaluated the effect of oxygen concentration on lipid oxidation denitively
show that the inuence of oxygen on lipid oxidation decreases with increasing oxygen concentration. That is, across a myriad of food systems oxygen concentrations below 12% strongly dictate
the rate of lipid oxidation because of oxidations dependency on the diffusion of oxygen. Nevertheless, research suggests that any decrease in oxygen concentration under atmospheric levels
(21%) will result in improved oxidative stability. Additional work is needed to better understand
the effect that oxygen concentrations ranging from 21% to 2% have on food systems. A pragmatic
strategy is to analyze the effect of very low oxygen concentrations because processes to eliminate
oxygen can lower the oxygen level of foods to <1.02.0%. Unfortunately, even this level of oxygen may still be able to trigger oxidative rancidity (Andersson & Lingnert 1997). Considering
this, measures must be taken to reduce the content of oxygen within a system to the lowest level
obtainable during food processing and packaging.
METHODS TO ENHANCE OXIDATIVE STABILITY

Currently, most strategies to enhance oxidative stability rely on antioxidants to combat free radicals
or prooxidative metals present in food systems. Recent trends to remove highly effective synthetic
antioxidants and utilize more natural antioxidants have made this strategy less practical; therefore,
new, or additional, methods of preventing oxidation of lipid components are needed. Oxygen
concentration is one of the most important extrinsic factors affecting lipid oxidation, and decreasing
it can lead to increased lipid stability. Physical methods for removing oxygen from packaging are
routinely employed in the food industry and focus on alteration of the gas contents of packaging.
Processing: Controlling Oxygen Level

Decreasing, and maintaining, low oxygen concentrations can be extremely effective in increasing
the shelf life of lipid-containing products. However, one must remember that these techniques
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are only effective prior to the consumer opening the product, with the exception of single-serve
food containers.
Nitrogen Flushing/Purging

One strategy to reduce the oxygen concentration of foods containing oil is to ush inert gases,
typically nitrogen, into the package to displace oxygen. Nitrogen ushing is particularly useful
for extending oxidative stability in fragile foods (e.g., potato chips) or displacing the air in the
headspace above foods. Lloyd et al. (2009) showed that nitrogen ushing of packaged whole milk
powder could reduce the peroxide and volatile formation when stored in the dark compared to a
nonushed control. Findings by Pristouri et al. (2010) show that large headspace oxygen volumes
contribute to substantial quality deterioration in bottled extra virgin olive oil. Sionek et al. (2013)
showed that removal of the oxygen reservoir, via nitrogen headspace ushing, could reduce the
formation of primary lipid reaction products (hydroperoxides) in rened rapeseed oil by 22%.
Nitrogen purging, bubbling the inert gas through the liquid phase, can also improve oxidative
stability, as Masella et al. (2010) demonstrated when nitrogen purging of olive oil was able to
remove 50% of dissolved oxygen, signicantly reducing peroxide formation.
Modified Atmosphere Packaging

Shelf-life extension of foods can also be achieved by modied atmosphere packaging (MAP),
which changes the internal gas contents in packaged foods to limit the amount of oxygen. MAP is
routinely accomplished by pumping a food system with an inert gas, such as nitrogen or carbon
dioxide, to displace oxygen. MAP is similar to nitrogen ushing/purging, but the goal is to achieve
predetermined gas concentrations to maximize stability and food quality. For instance, Lund et al.
(2007) found that modifying a package of beef patties in chilled storage to 100% nitrogen decreased
lipid oxidation, as measured by TBARS, by more than 70% compared to patties stored in MAP
with 80% oxygen.
Vacuum Packaging
The most complete removal of oxygen, vacuum packaging, involves air removal and a hermetic
seal so that a near perfect vacuum is achieved inside the food container. Nam & Ahn (2003) demonstrated that vacuum packaging of meats signicantly reduced lipid oxidation products compared
to atmospherically stored samples.
Removal of oxygen from the enclosed food system is necessary for improved stability, but the
packaging materials that determine gas transfer with the outside environment are equally important. Materials used in edible oil packaging are chosen on the basis of their weight, ease of handling,
avor absorption, and oxygen transmission rate (OTR) (Table 3). Recently, the use of plastic and
paperboard packaging has increased over glass and metals due to lower costs, low weight, and ease
of handling. However, because plastic and paperboard packaging allow oxygen transmission, they
are sometimes modied (e.g., aluminum foil lamination) to limit the amount of oxygen that can
permeate into the product (Piergiovanni & Limbo 2009). Additionally, oxygen ingress can occur
through package linings (e.g., seals and caps), allowing oxygen to enter the product. Another
hurdle in edible oil stability is that regardless of the oxygen removal method and type of package,
residual oxygen may still remain. Typically, ushing with an inert gas, MAP, and vacuum packaging leaves behind 2.05.0%, 0.91.1%, and 0.110.15% residual oxygen, respectively (Smiddy
et al. 2002, Warmbier & Wolf 1976). Additionally, it is imperative that a packaging material with
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Table 3 Packaging material OTRs (Lange & Wyser 2003; Duncan 2011)a
Oxygen permeability (cm3 mm/m2 day atm)
Packaging material
Glass
Negligible
Metal (aluminum sheet)
Negligible
PET
15
PVC
28
PE
50200

a
Abbreviations: OTRs, oxygen transmission rates; PE, poly(ethylene); PET, poly(ethylene terephthalate);
PVC, poly(vinyl chloride).
a negligible OTR (e.g., glass or a metal laminate layer) be used when oxygen removal techniques
are employed. To illustrate this point, imagine a low-moisture food (e.g., crackers or ready-to-eat
cereal) is packaged in plastic (from Table 3, surface area 1,600 cm2 ) and then subjected to a
process that removes all oxygen. A conservative estimate would be that within approximately
2432 days the headspace oxygen concentration would return to full atmospheric concentration
(21.0%) in the absence of a metal laminate layer. Using this knowledge, industry should consider
the efcacy of oxygen removal techniques when utilizing packaging with a high OTR.
Oxygen Scavengers
Oxygen scavengers can be employed to completely remove residual oxygen from the system.
Either edible oxygen scavengers or oxygen-absorbing sachets can be incorporated to reduce the
oxygen content to less than 0.01% (Cruz et al. 2012). Oxygen scavengers can be used in addition
to processing techniques, or as stand-alone scavengers, to reduce the costs associated with the
oxygen removal process. Scavengers can also be incorporated into packaging by dissolving them
in plastics used for bottle manufacture. Cecchi et al. (2010) demonstrated the efcacy of an oxygen
R
, dispersed within the plastic poly(ethylene terephthalate) (PET) that
scavenger catalyst, Amosorb
decreased peroxide formation by 18% in olive oil stored in light and evaluated after 13 months.
Importantly, the oxygen diffusivity of the packaging material, and the amount of oxygen present
in the sealed system upon manufacture, must be accounted for when calculating the amount of
scavengers needed to achieve, and maintain, an oxygen-free package.
Iron-Based Oxygen Scavenging

Metallic-reducing agents such as iron oxide, ferrous carbonate, and metallic platinum are commonly used in the food industry to scavenge oxygen. Iron-based scavengers work by the preferred
oxidation of iron to consume oxygen present in the enclosed package (Scheme 3). Generally, in
commercial scavengers 1 g of iron can scavenge approximately 300 mL of oxygen (Cruz et al.
2012). The scavengers are packaged in small sachets to partition the reactive metals away from
Fe Fe2+ + 2 e
O2 + H2O + 2 e 2 OH
Fe2+ + 2 OH Fe(OH)2
Fe(OH)2 + O2 + H2O Fe(OH)3
Scheme 3
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sensitive food ingredients and prevent ingestion of toxic components. In a cracker system, an iron
oxide scavenger was able to reduce the level of oxygen from 21% to 3.0% within one day and was
able to extend sensory acceptance by more than 20 weeks (Berenzon & Saguy 1998). Mexis &
Kontominas (2010) showed that iron-based oxygen absorbers could extend the oxidative stability
of almonds regardless of storage temperature and initial oxygen concentrations. However, ironbased scavengers have drawbacks due to their toxicity, sachet storage, and also their ability to set
off metal detectors.
Enzyme-Based Oxygen Scavenging

Other oxygen scavengers function enzymatically, such as the glucose oxidase-catalase system,
to remove oxygen from the environment. Glucose oxidase donates hydrogen atoms from the
CHOH group of glucose to oxygen, forming a glucono-delta-lactone and hydrogen peroxide:
2 glucose + 2 O2 + 2 H2 O 2 gluconic acid + 2 H2 O2 (Labuza & Breene 1989). However,
hydrogen peroxide must be reduced to water and oxygen to prevent decomposition into free
radicals that promote lipid oxidation: 2 H2 O2 + catalase 2 H2 O + O2 . Thus, the system becomes
inefcient in reducing oxygen. Another disadvantage to this system is that it is very sensitive to
changes in pH, water activity, temperature, and salinity. Moreover, Min et al. (2003) found that
glucose oxidase-catalase acted as an antioxidant at lower concentrations in salad dressing, but at
higher concentrations above 0.3 unit/g, there was a prooxidative effect. The prooxidant effect
results potentially from the increased concentration of prooxidative heme groups from catalase
or by free radicals produced from hydrogen peroxide decomposition. Due to the drawbacks of
glucose oxidase-catalase, it is often only used under a narrow range of food products such as beer
and wine bottle caps.
Ascorbate Oxygen Scavenging

An alternative edible oxygen scavenger that has been gaining attention due to its safety, natural
label, and efcacy is ascorbic acid. Ascorbic acid is able to scavenge oxygen by an oxidation reaction
that produces dehydroascorbic acid (DHAA) (Scheme 4). The complete reduction of 1 mol of
atmospheric oxygen requires 2 mol of ascorbic acid and results in the formation of DHAA and
water. This reaction reduces the level of oxygen over the course of days, but can be accelerated
by transition metals and light (Cruz et al. 2012). In model aqueous solutions, 3.43.6 mg ascorbic
acid can scavenge the oxygen in 1 cm3 of headspace air, which is close to the theoretical value of
3.3 mg cm3 (Cort 1982). Ascorbic acid can also be conjugated to a fatty acid, such as palmitic
acid (ascorbyl palmitate), to increase its solubility in lipid systems. Researchers debate the efcacy
of ascorbyl palmitate because it may be difcult to reach high enough concentrations to scavenge
substantial amounts of oxygen because of solubility constraints in some foods (Cort 1982, Frankel
2005). A drawback to using ascorbate in oxygen scavenging applications is its ability to reduce ferric
AA + 2 Cu2+ (or Fe3+) DHAA + 2 Cu+ (or Fe2+) + 2 H+
2 Cu+ (or Fe2+) + 2 O2 2 Cu2+ (or Fe3+) + 2 O2
2 O2 + 2 H+ + Cu2+ (or Fe3+) O2 + H2O2 + 2 Cu2+ (or Fe3+)
H2O2 + Cu2+ (or Fe3+) + AA Cu2+ (or Fe3+) + DHAA + 2 H2O
Net: AA + O2 DHAA + H2O

Scheme 4
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Metal chelator
FRS
LOH
FRS

O2
2H2O
2AA
Fe3+
LO
2DHAA
Fe2+
LOOH
Radical attack
Figure 3
Ascorbic acid interacting in a complex system with the capacity to scavenge environmental oxygen (left).
Ascorbic acid also possesses potential prooxidative properties by recycling metals to their more active form,
causing free radical generation (middle). Metal chelators and FRS can be employed to decrease potential lipid
oxidation initiating events (right). Abbreviations: AA, ascorbic acid; DHAA, dehydroascorbic acid; FRS, free
radical scavengers.
iron to the more prooxidative ferrous state (Alamed et al. 2009). Thus, the relationship between
ascorbic acid and oxygen scavenging is contradictory. Trace metals must be present within the
system to help catalyze the scavenging reaction, but the transition metals (iron and copper) need
to be chelated or ascorbate could increase oxidation rates (Figure 3).
Sulfite Oxygen Scavenging

Other edible scavengers include sultes that have been incorporated into packaging material and
possess enough thermal stability to maintain their efcacy after thermoplastic processing (Cruz
et al. 2012). The drawback to sulte usage is that oxygen scavenging can produce sulfur dioxide
as a by-product, which decreases the sensory acceptability of the product and may pose allergenic
concerns (Brody et al. 2001).
MEASURING OXYGEN CONCENTRATION

Measuring oxygen concentration and diffusivity helps to identify a critical substrate that can impact all oxidative reactions in foods. However, data on oxygen within food systems are difcult to
obtain. Interference of atmospheric oxygen during sampling and oxygen consumption in chemical
reactions are two obstacles facing oxygen measurements in foods. Most of the techniques used
today have been available since the 1950s, each with its own utility. The Winkler test, commonly
used to calibrate other methods, chemically reacts with oxygen to quantify oxygen in water via
colorimetric titration of iodine. The Winkler test is not suitable for complex foods containing
components that can oxidize or reduce iodine, such as hydroperoxides. Gravimetry is used to
measure the global system oxygen gain by monitoring weight changes, but mass loss due to volatiles
cannot be differentiated from oxygen changes. Manometric and volumetric oxygen analysis methods are the oldest means of quantifying oxygen and measuring the difference in total pressure or
total volume, respectively. Many early studies used manometry as the basis of determining oxygen
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solubility in oils (Penicaud et al. 2012). However, problems arise because signicant amounts of
pressure or volume changes are needed and contamination from atmospheric gases is common.
Oxygen and its stable radicals can be directly measured by the interaction between the biradical
of triplet oxygen and a magnetic eld via electron paramagnetic resonance (EPR). Wagner et al.
(1994) used EPR in combination with an oxygen monitor to follow the generation of lipid-derived
free radicals during lipid peroxidation in cells. Unfortunately, technical challenges and the cost of
instrumentation have limited EPR use for quantifying oxygen. Electrochemical methods, such as
the Clark electrode, have also been used to quantify oxygen in foods (Ohashi et al. 1994). Oxygen
determination is achieved when the sample is submitted to an electrochemical potential difference
causing oxygen to be reduced to hydroxide ions. The hydroxide ions generate an electric current
proportional to the oxygen chemical potential, but the procedure requires calibration to correlate
to oxygen concentration. The major disadvantage of electrochemical measurements is that
oxygen consumption during determination prevents the ability to measure continuously. Gas
chromatography is a widely used method to monitor oxygen levels, with the major limitation
being its ability to perform only headspace analysis (Andersson & Lingnert 1997).
The most recent advance in oxygen quantication is the use of luminescent dyes that are
specically sensitive to oxygen. Luminescent dyes can be used to quantify oxygen in foods based
on energy transfer from the ruthenium-containing uorophore to oxygen (Tikekar et al. 2011),
which decreases the intensity of uorescence with increasing oxygen content (Penicaud et al.
2010). The system is calibrated against atmospheric oxygen and expresses oxygen as a partial
pressure. A ber optic cable probe can be added to this system to simultaneously detect dissolved
or headspace oxygen concentration (Figure 4). Optical probes appear to be the most versatile
given that they do not consume oxygen, are sensitive to low levels of oxygen, provide continuous

FO06CH08-Decker
Headspace
oxygen
O2 sensing patch
with rutheniumcontaining dye
Dissolved oxygen
in sample
Transmitter
Fiber optic
cable probe
Transmitter
Figure 4
Example of a noninvasive experimental setup for simultaneous analysis of dissolved and headspace oxygen
using a ruthenium-containing dye and a ber optic cable probe (modied with permission from Chaix et al.
2014).
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analysis, and have fast response times (Garca-Torres et al. 2009). The drawbacks associated
with this method are derived from its sensitivity to photobleaching of the ruthenium-containing
uorophore and position dependence of the ber optic cable. Smiddy et al. (2002) used optical
oxygen probes to continuously monitor oxygen levels in packaged meats to demonstrate that the
shelf life of MAP chicken patties was less oxidatively stable than vacuum packed samples. More
in-depth discussions of analytical techniques measuring oxygen solubility and diffusivity in foods
are provided in recently completed reviews by Penicaud et al. (2012) and Chaix et al. (2014).

CONCLUSION
This review has highlighted the importance of oxygen content and location in determining the
oxidative stability of lipid-containing foods. Our understanding is that any decrease in oxygen
content is advantageous in protecting oxidatively susceptible foods. However, the relative inuence
of oxygen becomes greater as lower and lower oxygen concentrations are reached. The importance
of very low levels of oxygen (i.e., <12% oxygen) for extending shelf life has been shown; however,
any residual oxygen will still eventually allow lipid oxidation to proceed. Practically speaking, a
complete removal of oxygen in some food systems may not be feasible. Thus more knowledge
regarding lipid oxidation in the 12% oxygen range is needed to determine resources necessary to
process and package oxygen-sensitive foods. Further studies are also needed to detail the effects of
varying oxygen contents and their relationship to various pro/antioxidants in foods. For example,
would oxygen reduction be more effective in foods susceptible to singlet oxygen degradation or
in food systems whose stability is dependent on metal-promoted oxidation?
Reaching oxygen concentrations below 2% could be difcult and/or expensive for many foods.
It might be more feasible to use combinations of technologies such as nitrogen ushing with edible
oxygen scavenging such as ascorbic acid. However, before these combinations can be used, more
research is needed to determine conditions where residual antioxidants (e.g., ascorbic acid) would
not be prooxidative. Controlling oxygen concentrations could also help enhance the activity of
natural antioxidants such that their effectiveness could be similar to that of synthetic antioxidants.
Antioxidant applications incorporating knowledge explained in this review are needed, especially
as the food industry faces the major challenge of increasing incorporation of healthy, but also
unstable, polyunsaturated fatty acids.
DISCLOSURE STATEMENT
The authors are not aware of any afliations, memberships, funding, or nancial holdings that
might be perceived as affecting the objectivity of this review.
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Annual Review
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Contents
Volume 6, 2015
An Amazing Journey
Larry McKay p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
Physical Modication of Food Starch Functionalities
James N. BeMiller and Kerry C. Huber p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p19
Nanostructured Fat Crystal Systems
Nuria C. Acevedo and Alejandro G. Marangoni p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p71
Antimicrobial Food Equipment Coatings: Applications and Challenges
Luis J. Bastarrachea, Anna Denis-Rohr, and Julie M. Goddard p p p p p p p p p p p p p p p p p p p p p p p p p p p97
Non-Nutritive Sweeteners and Obesity
John D. Fernstrom p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 119
Genetic Mechanisms of Prebiotic Oligosaccharide Metabolism in
Probiotic Microbes
Yong Jun Goh and Todd R. Klaenhammer p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 137
Electrostatic Coating Technologies for Food Processing
Sheryl A. Barringer and Nutsuda Sumonsiri p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 157
The Role of Oxygen in Lipid Oxidation Reactions: A Review
David R. Johnson and Eric A. Decker p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 171
Stress Adaptation in Foodborne Pathogens
Maire Begley and Colin Hill p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 191
Colloids in Food: Ingredients, Structure, and Stability
Eric Dickinson p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 211
Antihypertensive Peptides from Food Proteins
Rotimi E. Aluko p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 235
Pickering Emulsions for Food Applications: Background, Trends, and Challenges
Claire C. Berton-Carabin and Karin Schroen p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 263
The Nutraceutical Bioavailability Classication Scheme: Classifying Nutraceuticals
According to Factors Limiting their Oral Bioavailability
David Julian McClements, Fang Li, and Hang Xiao p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 299
v
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Comparative Analysis of Intestinal Tract Models

C.F. Williams, G.E. Walton, L. Jiang, S. Plummer, I. Garaiova,
and G.R. Gibson p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 329
Bacillus and Other Spore-Forming Genera: Variations in Responses
and Mechanisms for Survival
Aleksandra Checinska, Andrzej Paszczynski, and Malcolm Burbank p p p p p p p p p p p p p p p p p p p p 351
Protein-Polysaccharide Interactions to Alter Texture
Fred van de Velde, Els H.A. de Hoog, Alexander Oosterveld, and R. Hans Tromp p p p p p 371
High Hydrostatic Pressure Processing: A Promising Nonthermal

Technology to Inactivate Viruses in High-Risk Foods
Fangfei Lou, Hudaa Neetoo, Haiqiang Chen, and Jianrong Li p p p p p p p p p p p p p p p p p p p p p p p p p p 389
Human Norovirus as a Foodborne Pathogen: Challenges
and Developments
Matthew D. Moore, Rebecca M. Goulter, and Lee-Ann Jaykus p p p p p p p p p p p p p p p p p p p p p p p p p p 411
Principles and Application of High PressureBased Technologies in
the Food Industry
V.M. (Bala) Balasubramaniam, Sergio I. Martnez-Monteagudo,
and Rockendra Gupta p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 435
Challenges and Solutions to Incorporation of Nutraceuticals in Foods
Mary Ann Augustin and Luz Sanguansri p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 463
Statistical Aspects of Food Safety Sampling
I. Jongenburger, H.M.W. den Besten, and M.H. Zwietering p p p p p p p p p p p p p p p p p p p p p p p p p p p p 479
Diet-Based Strategies for Cancer Chemoprevention: The Role of
Combination Regimens Using Dietary Bioactive Components
Christina DiMarco-Crook and Hang Xiao p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 505
Collagen and Gelatin
Dasong Liu, Mehdi Nikoo, Gokhan Boran, Peng Zhou, and Joe M. Regenstein p p p p p p p p 527
Indexes
Cumulative Index of Contributing Authors, Volumes 16 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 559
Cumulative Index of Article Titles, Volumes 16 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 562
Errata
An online log of corrections to Annual Review of Food Science and Technology articles may
be found at http://www.annualreviews.org/errata/food
vi
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