The effect of lipid oxidation on the quality of meat and meat products

Michaela Králová
Department of Milk Hygiene and Technology
Faculty of Veterinary Hygiene and Ecology
University of Veterinary and Pharmaceutical Sciences in Brno
Brno, Czech Republic

Abstract

Lipid oxidation is currently one of the greatest economic problems facing the meat industry.
It is one of the main causes of deterioration in the quality of meat and meat products during their
storage and processing. Meat oxidation causes discoloration, the development of off-flavour, the
formation of toxic compounds, reduced shelf life and nutrient losses. Meat becomes susceptible
to oxidative deterioration due to high concentrations of unsaturated lipids, haem pigments, metal
catalysts and a range of oxidising agents contained in the muscle tissue. Autoxidation is of the
greatest significance. This takes place in three stages – initiation, propagation and termination.
A large variety of volatiles, including alkanes, aldehydes, alcohols, esters and carboxylic acids,
arise from this process. The aim of this study is to summarise current knowledge about the effect
of lipid oxidation on the quality of meat and meat products and the use of natural antioxidants
which are becoming increasingly important.

Lipids, meat, oxidation,rancidity

Introduction

Meat and meat products are susceptible to deterioration in view of their rich nutritional
composition (Devatkal et al. 2012). This deterioration occurs as the result of a number
of chemical and microbial changes. The most common form of chemical damage is lipid
oxidation in meat (Medina-Meza et al. 2014; Shah et al. 2014). Lipid oxidation is an
important factor limiting both the quality of meat products and their acceptability to the
customer. Food become unacceptable to the consumer once a certain degree of rancidity is
attained (Sammet et al. 2006). Lipid oxidation is a complex process that is dependent on
the chemical composition of the meat, the presence of light and oxygen, and on the storage
temperature (Belitz et al. 2004). It is also influenced by certain technological procedures
to which meat is subjected during processing (Falowo et al. 2014; Medina-Meza et al.
2014). During the course of lipid oxidation, a number of compounds are formed that have
an influence on the quality of meat and meat products expressed in the form of sensory
changes (colour, texture and taste) and a deterioration of nutritional quality (Min and
Ahn 2005; Karre et al. 2013). Lipid oxidation in meat and meat products may be reduced
or inhibited by antioxidants, thereby ensuring improved product quality and an extended
storage period (Shah et al. 2014). The aim of this study is to assess the mechanism and
influence of lipid oxidation on the quality of meat and meat products and to evaluate the use
of the antioxidants, largely of natural origin, that are currently being used to a continually
increasing extent.
Lipid oxidation
All foods that contain lipids, even in extremely small quantities (< 1%), may undergo
oxidation which leads to the onset of rancidity (Wąsowicz et al. 2004).
Oxidation involves reactions of the hydrocarbon chains that are common to free fatty acids
and their esters. The carboxyl of free fatty acids, however, speeds up the decomposition of
hydroperoxides and may react with certain oxidation products. A number of types of lipid
Address for correspondence:
MVDr. Michaela Králová, Ph.D.
Department of Milk Hygiene and Technology
Faculty of Veterinary Hygiene and Ecology Phone: +420 541 562 714
University of Veterinary and Pharmaceutical Sciences Brno E-mail: kralovam@vfu.cz
Palackého tř. 1946/1, 612 42 Brno, Czech Republic www.maso-international.cz
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oxidation reaction may take place in foods, such as autoxidation with atmospheric oxygen,
oxidation with hydroperoxides or hydrogen peroxide, oxidation with singlet oxygen during
photo-oxidation, oxidation catalysed by enzymes (lipoxygenases), oxidation with heavy
metals at a higher valence, and oxidation with quinones and related compounds (Velíšek
and Hajšlová 2009).The most important mechanisms of oxidation are given in Table 1
with the type of oxidation, precursors and primary products.

Table 1. Mechanisms of lipid oxidation (Pokorný 2006)

Type of oxidation Precursors Primary products

Catalysed by lipoxygenase Linoleic and linolenic acid Conjugated hydroperoxides
Autoxidation Unsaturated fatty acids Hydroperoxides
Photo-oxidation Unsaturated fatty acids Hydroperoxides
In vivo oxidation Essential fatty acids Eicosanoids
Hydrogen peroxide oxidation Unsaturated fatty acids Hydroxy acids

The commonest type of oxidation during the processing and storage of meat and meat
products (and foodstuffs in general) is the autoxidation of fatty acids (Gandemer 2002;
Santos-Fandila et al. 2014). Only unsaturated fatty acids are oxidised by atmospheric
oxygen at ordinary temperatures. Saturated fatty acids enter the autoxidation process at
higher temperatures associated with processing methods such as boiling, baking, frying,
roasting, etc. (Velíšek and Hajšlová 2009; Resconi et al. 2013). This is due to various
degrees of bond dissociation energy at various positions in fatty acids (Table 2).
Table 2. Bond dissociation energy of hydrogen at various positions in the carbon chain (Belitz et al. 2004;
Zuleta et al. 2012)

Position of hydrogen E [kJ·mol-1]

H-CH2- 422
CH3-HCH- 410
R-HCH-CH=CH- 322
R-CH=CH-HCH-CH=CH- 272

Autooxidation
Mechanism
The autoxidation of lipids associated with the production of free radicals is a spontaneous
reaction of atmospheric oxygen with fatty acids that leads to oxidative damage to meat
and meat products and the formation of undesirable sensory properties (Wąsowicz
et al. 2004; Dave and Ghaly 2011; Santos-Fandila et al. 2014). Autoxidation takes
place as a radical chain reaction characterised by three steps – initiation, propagation and
termination (Falowo et al. 2014; Santos-Fandila et al. 2014).

• Initiation
During initiation, the homolytic cleavage of the covalent bond in the C-H hydrocarbon
chain takes place with the formation of a free hydrogen radical (H•) and fatty acid free
radical (R•) (1) (Velíšek and Hajšlová 2009). Catalysts of this reaction include heating,
radiation, metal ions and other free radicals (Hájek et al. 1998; Dave and Ghaly 2011).

RH → R• + H• (1)
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Cleavage also occurs by means of a reaction with another free radical or a reaction with
metals with transitory valence (Velíšek and Hajšlová 2009).

• Propagation
A reaction occurs in the second step of autoxidation between the highly reactive fatty
acid radical and atmospheric oxygen to form a highly reactive peroxyl radical (ROO•) (2)
which is capable of reacting with unsaturated fatty acids to form hydroperoxides (ROOH)
(3) (Wąsowicz et al. 2004; Velíšek and Hajšlová 2009).

R• + O2 → ROO•  (2)

ROO• + RH → ROOH + R• (3)

The sequence of two given reactions may be repeated a number of times, for which
reason autoxidation is known as a  chain reaction (Velíšek and Hajšlová 2009).
The reaction of a fatty acid free radical with oxygen is far quicker than the reaction between
a peroxyl radical and a lipid hydrocarbon chain. The second reaction therefore determines
the speed of autoxidation (Wąsowicz et al. 2004; Velíšek and Hajšlová 2009).

• Termination
In the final phase of autoxidation, i.e. termination, non-radical relatively stable products
are formed if the concentration of free radicals is sufficiently high (4, 5 and 6) (Wąsowicz
et al. 2004; Velíšek and Hajšlová 2009; Dave and Ghaly 2011).

R• + R• → R-R  (4)

R• + ROO• → ROOR  (5)

ROO• + ROO• → ROOR + O2  (6)

If the availability of oxygen is restricted, when the speed of autoxidation depends

on its partial pressure, the main radicals in the system are fatty acid radicals and the
main termination reaction is their recombination (4). If sufficient oxygen is available,
the reaction speed is not dependent on its partial pressure and more peroxyl radicals
are formed. The main reactions are then the recombination of fatty acid radicals with
peroxyl radicals and the mutual recombination of peroxyl radicals (5, 6) (Vel í šek and
Hajšlová 2009).
Products of autoxidation
The oxidation of lipids, and of unsaturated fatty acids in particular, leads to the formation
of hydroperoxides whose cleavage is accompanied by the formation of secondary products
such as pentanal, hexanal, 4-hydroxynonenal, malondialdehyde and other oxygen
compounds including aldehydes, acids and ketones (Fernández et al. 1997). These
secondary products may cause loss of colour and nutritional value and a negative smell
and taste (Min and Ahn 2005; Resconi et al. 2013) due to their effect on lipids, pigments,
proteins, saccharides and vitamins (Fernández et al. 1997; Dave and Ghaly 2011).
They are often associated with toxic effects (the inception of atherosclerosis, carcinogenic
and mutagenic properties) (Sammet et al. 2006; Dave and Ghaly 2011; Duthie et al.
2013). In certain cases, oxidation products may contribute to the typical aroma of the
given products (Gandemer 2002). An overview of cleavage products formed during lipid
oxidation is given in Fig. 1.
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• Primary products
The primary products of autoxidation are hydroperoxides (Fernández et al. 1997;
Wąsowicz et al. 2004; Reconi et al. 2013). Hydroperoxides, and hydroperoxides of
diene and triene acids in particular, are highly unstable and eliminate either a hydrogen
radical to form a peroxyl radical or a hydroxyl radical to form an alkoxyl radical (Velíšek
and Hajšlová 2009). Peroxyl and alkoxyl radicals are highly reactive and can therefore
act as initiators of autoxidation (Wąsowicz et al. 2004).

• Secondary products
The decomposition of fatty acid hydroperoxides and their radicals may lead to the
formation of various products in secondary reactions (Santos-Fandila et al. 2014). Three
types of reaction can differentiated (Velíšek and Hajšlová 2009).
1. Reactions that do not lead to a change in the number of carbon atoms in the molecule
(e.g. the formation of cyclic peroxides and endoperoxides, epoxy acids, hydroxy acids
and oxoacids).
2. Reactions in which decomposition of the molecule occurs with the formation of products
with a smaller number of carbon atoms (e.g. reactions forming aldehydes, hydrocarbons
or oxoacids).
3. Polymerisation reactions (an increase to the number of carbons in the molecule).

Fig. 1. The mechanism of lipid oxidation (Santos-Fandila et al. 2014; amended)

Factors influencing the lipid oxidation

The speed of lipid autoxidation depends on a number of factors, e.g. the composition of
fatty acids (polyunsaturated fatty acids are more susceptible), the presence of antioxidants,
pro-oxidants, etc. (Dave and Ghaly 2011; Falowo et al. 2014). An overview of the
factors influencing the course of autoxidation is given in Table 3.
Min et al. (2008) and Min and Ahn (2005) state that the susceptibility of meat to the
oxidation is also influenced by the animal species, the breed, the type of muscle and its
anatomical location.
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Table 3. Factors influencing the rate and course of lipid oxidation (Belitz et al. 2004; Schaich et al. 2013, amended)

Nature of the lipids Degree of unsaturation, free fatty acids vs esters vs TAGs, trans vs cis, conjugation, phospholipids
Surface effects Dispersion, emulsion
Presence of catalysts Pro-oxidants (hydroperoxides, metals, porphyrins, heme compounds), enzymes (lipoxygenase,
cyclooxygenase, xanthine oxidase), amino acids, ascorbic acid (low concentrations)
Presence of inhibitors Antioxidants (endogenic and exogenic), polyphenols, metal chelators, synergists, amino acids,
enzymes (glutathione peroxidase), interceptors (proteins, DNA, vitamins, pigments)
Environment Temperature, light, partial oxygen pressure, water, pH, packaging

Antioxidants
Modified atmospheres and antioxidants are used to prevent or delay lipid oxidation
(Sammet et al. 2006). Antioxidants are substances that extend the durability of foods and
protect them against spoilage caused by oxidation that may take the form of fat rancidity or
colour changes in foods (Decree No. 4/2008 Coll.).

Fig. 2. The interaction between the induction of oxidation and the potential of natural antioxidants to prevent
the oxidation of meat (Falowo et al. 2014, amended)
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Antioxidants interfere with the process of the oxidation of lipids and other oxylabile
compounds by reacting with free radicals (primary antioxidants) or reducing any
hydroperoxides formed (secondary antioxidants). They also bind to complexes of transition
metals and eliminate oxygen present (Wąsowicz et al. 2004; Velíšek and Hajšlová
2009; Dave and Ghaly 2011).

Table 4. Plant sources used as natural antioxidants in the production of meat and meat products (Falowo et al. 2014
and Shah et al. 2014, amended)

Part of plant Source

Leaves and secondary branches Rosemary, hyssop
Leaf Rosemary, nettle, mint, lotus, myrtle, lemon balm, oregano, lemon grass, summer savory, curry,
butterbur, Chinese chives/leek, daisy, pumpkin, sesame, soybean, thyme, olive
Flower Nettle
Peel Pomegranate, potato
Rhizome Ginger, lotus
Flowering head Broccoli
Seed Grape
Aerial parts Garlic
Bulb Garlic, onion
Bark Cinnamon

In view of possible side effects, an effort is being made to reduce the use of synthetic
antioxidants in view of their reduced acceptability among customers (Falowo et al. 2014)
and to use natural antioxidants (Shah et al. 2014).

Table 5. Commercially available natural antioxidants of plant origin applied in the production of meat and meat products
(Falowo et al. 2014; Shah et al. 2014, amended)

Extract Tested meat / meat product

Grape seed extract Ground beef, beef frankfurters, beef and pork meat, beef and pork patties,
frozen pork patties, ground goat meat, restructured mutton slices
White grape extract Chilled beef patties
Grape skin extract Pork patties
Pine bark extract Ground beef
Green tea extract (catechins) Pork sausages
Green tea extract Pork patties
Coffee extract Pork patties
Green coffee antioxidant Pork sausages
Olive leaf extract Beef, pork patties, pork sausages
Water-soluble oregano extract Beef and pork patties
Adzuki bean extract Pork sausages
Rosemary oleoresin Beef and pork patties, ground beef
Rosemary extract Boerewors-South African fresh sausage, pork sausages, pork patties
Carob fruit extract Cooked pork
Broccoli powder extract Goat meat nugget
Avocado seed extract Pork patties
Ginkgo biloba leaf extract Meat dumplings
Herbal extracts (marjoram, rosemary) Ground beef
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The rate and extent of oxidation may be limited, reduced or halted by the use of natural
antioxidants (Fig. 2) (Falowo et al. 2014). For example, Sammet et al. (2006) assessed
the effect of α-tocopherol supplementation in the diet of pigs whose meat was used for
the production of salami. A concentration twice as high was found in these products in
comparison with a control group.
Technological strategies include the application of antioxidants directly to meat and
meat products and the application of plant extracts to packaging material with the aim of
achieving greater product stability (Falowo et al. 2014).
Natural antioxidants are obtained from plant sources such as herbs, roots, vegetables,
fruit and oleaginous products (Shahidi and Zhong 2010). Natural antioxidants come
from various parts of plants, such as leaves, roots, stems, fruits, seeds, skin and bark
(Shah et al. 2014). An overview of plant sources used as natural antioxidants is given in
Table 4. Some of these antioxidants are used commercially in the meat industry and their
specific applications are given in Table 5. Many natural antioxidants, e.g. rosemary and
spice extracts, have been described as being more effective than synthetic antioxidants. It is
important that further research will be focused on their use in the production of foodstuffs
(Karre et al. 2013). The use of antioxidants in food products is a  subject stated in the
national legislation and international standards (Decree No. 4/2004; Karre et al. 2013).
The use of natural antioxidants in meat and meat products during processing and
storage can be considered multifunctional in view of their antioxidant, antimicrobial
and preservative effects. The addition of natural antioxidants stabilises cholesterol
levels, inhibits the formation of its oxidation products, and reduces the formation and
absorption of malondialdehyde and heterocyclic amines in heat-treated meat
(Falowo et al. 2014).

Conclusions
Lipid oxidation in meat and meat products is the main cause of their deterioration. A large
number of compounds formed during autoxidation have a  negative effect on the taste,
aroma and safety of meat products, reduce their nutritional value and shorten their shelf
life. Antioxidants can be used to prevent oxidation processes. Efforts are currently being
made to restrict the use of synthetic antioxidants in view of their possible toxic effects
and to replace them with natural antioxidants which become more and more interesting
for the consumer. These natural antioxidants, rich in phenolic substances, are obtained
from various parts of plants, such as leaves, roots, stems, seeds, etc. and provide a suitable
alternative to synthetic antioxidants.
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