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MEAT
SCIENCE
Meat Science 74 (2006) 17–33
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Review
Innovations in beef production systems that enhance the nutritional and
health value of beef lipids and their relationship with meat quality
Nigel Scollan
a
a,*
, Jean-François Hocquette b, Karin Nuernberg c, Dirk Dannenberger c,
Ian Richardson d, Aidan Moloney e
Institute of Grassland and Environmental Research, Plas Gogerddan, Aberystwyth, Wales SY23 3EB, United Kingdom
b
INRA-Unité de Recherches sur les Herbivores, Theix, 63122 Saint-Genès-Champanelle, France
c
Institute for Biology of Farm Animals, Wilhelm-Stahl-Allee 2, D-18196 Dummerstorf, Germany
d
Division of Farm Animal Science, University of Bristol, Langford, England BS40 5DU, United Kingdom
e
Teagasc, Grange Research Centre, Dunsany, Co. Meath, Ireland
Received 7 April 2006; received in revised form 27 April 2006; accepted 2 May 2006
Abstract
Consumers are becoming more aware of the relationships between diet and health and this has increased consumer interest in the
nutritional value of foods. This is impacting on the demand for foods which contain functional components that play important roles
in health maintenance and disease prevention. For beef, much attention has been given to lipids. This paper reviews strategies for increasing the content of beneficial omega-3 polyunsaturated fatty acids (PUFA) and conjugated linoleic acid (CLA) and reducing saturated
fatty acids (SFA) in beef. Particular attention is given to intramuscular fat (IMF) and the relationships between fatty acid composition
and key meat quality parameters including colour shelf life and sensory attributes. Despite the high levels of ruminal biohydrogenation of
dietary PUFA, nutrition is the major route for increasing the content of beneficial fatty acids in beef. Feeding grass or concentrates containing linseed (rich in a-linolenic acid, 18:3n 3) in the diet increases the content of 18:3n 3 and its longer chain derivative eicosapentaenoic acid (EPA, 20:5n 3) in beef muscle and adipose tissue, resulting in a lower n 6:n 3 ratio. Grass feeding also
increases docasahexaenoic acid (DHA, 22:6n 3). Feeding PUFA rich lipids which are protected from ruminal biohydrogenation result
in further enhancement of the PUFA in meat with concomitant beneficial improvements in the ratio of polyunsaturated:saturated fatty
acids (P:S ratio) and n 6:n 3 ratio. The main CLA isomer in beef is CLA cis-9, trans-11 and it is mainly associated with the triacylglycerol lipid fraction and therefore is positively correlated with level of fatness. The level of CLA cis-9, trans-11 in beef is related to (1)
the amount of this isomer produced in the rumen and (2) synthesis in the tissue, by delta-9 desaturase, from ruminally produced trans
vaccenic acid (18:1 trans-11; TVA). Feeding PUFA-rich diets increases the content of CLA cis-9, trans-11 in beef. Trans-fatty acids in
foods are of rising importance and knowledge of the differential effects of the individual trans isomers is increasing. TVA is the major
trans 18:1 isomer in beef and as the precursor for tissue CLA in both animals and man should be considered as a neutral or beneficial
trans-isomer. Increasing the content of n 3 PUFA in beef can influence colour shelf life and sensory attributes of the meat. As the content of n 3 PUFA increases then sensory attributes such as ‘‘greasy’’ and ‘‘fishy’’ score higher and colour shelf life may be reduced.
Under these situations, high levels of vitamin E are necessary to help stabilise the effects of incorporating high levels of long chain PUFA
into meat. However, grass feeding not only increases n 3 PUFA and CLA but, due to its high content of vitamin E, colour shelf life is
improved. It is evident that opportunities exist to enhance the content of health promoting fatty acids in beef and beef products offering
opportunities to add value and contribute to market differentiation. However, it is imperative that these approaches to deliver ‘‘functional’’ attributes do not compromise on the health value (lipoperoxidation) or the taste of beef products.
2006 Elsevier Ltd. All rights reserved.
Keywords: Beef; Nutrition; Meat quality; Fatty acids; Health
*
Corresponding author. Tel.: +44 1970 823075; fax: +44 1970 828357.
E-mail address: [email protected] (N. Scollan).
0309-1740/$ - see front matter 2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.meatsci.2006.05.002
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N. Scollan et al. / Meat Science 74 (2006) 17–33
Contents
1.
2.
3.
4.
5.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Fat content and fatty acid composition of beef . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.1. Fatty acid profile of IMF and relationships to human health . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.2. Regulation of IMF deposition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.3. Genetic control of IMF accumulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Strategies influencing the fatty acid composition of beef . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.1. Forages and the fatty acid composition of beef . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.2. Supplementary lipids and the fatty acid composition of beef . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.2.1. Unprotected lipids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.2.2. Protected lipids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.3. Dietary effects on trans fatty acids in beef . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.4. Dietary effects on CLA in beef . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Fatty acids and meat quality. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.1. Meat flavour. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.2. Lipid and colour stability. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction
Consumer requirements for food which is safe, healthier, of consistent eating quality, diverse and convenient is
increasing. In response, the food industry, supported by
the research community, continues to drive new opportunities to address the needs of the consumer. In addition to
consumer related issues, increased globalisation, reduced
commodity prices, World Trade negotiations, increased
animal welfare concerns, the need for traceability and environmental legislation have increased pressure at various
points across the food chain. The primary producer in particular, has been most affected with considerable reductions
in profit margins. Competitiveness in developed food markets is linked to the ability to develop new differentiated
products which increasingly seek to move away from the
cost and price-based competition associated with commodity-driven markets (Grunnert, Bredahl, & Brunsø, 2004).
This is commonly accepted for food products which
require a higher degree of processing but it is increasingly
apparent in fresh foods, including meat (Grunnert et al.,
2004).
These trends are also occurring in the fresh beef market
as reflected in the demand for higher quality and the drive
to differentiate beef on the basis of product brandings, geographical origin, sensory or processing characteristics. Definition of quality is becoming increasingly complex as it
encompasses the physical intrinsic qualities of the meat
(colour, shape, appearance, tenderness, juiciness, flavour)
and extrinisic qualities (brand, quality mark, origin, healthiness, production environment etc.) (Steenkamp, 1997).
Consumers are increasingly aware of the relationships
between diet and health, particularly in relation to cancer,
atherosclerosis and obesity/type 2 diabetes. Knowledge of
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these relationships has augmented consumer interest in
the nutritional quality of food such that this is becoming
a more important dimension of product quality.
Beef is considered to be a highly nutritious and valued
food. The importance of meat as a source of high biological
value protein and micronutrients (including for example
vitamins A, B6, B12, D, E, iron, zinc, selenium) is well
recognised (Biesalski, 2005; Williamson, Foster, Stanner,
& Buttriss, 2005). However, over the last 10–15 years, these
positive attributes have often been overshadowed due to
the prominence given to several negative attributes. The
latter include the perception that beef contains high
amounts of fat which is rich in saturated fat, associations
between red meat and cancer and non-nutritional issues
such as animal health scares, i.e. BSE. The relationships
between dietary fat and incidence of lifestyle diseases, particularly coronary heart disease are well established and
this has contributed towards the development of specific
guidelines from the World Health Organisation in relation
to fat in the diet (WHO, 2003). It is recommended that
total fat, saturated fatty acids (SFA), n 6 polyunsaturated fatty acids (PUFA), n 3 PUFA and trans fatty
acids should contribute <15–30%, <10%, <5–8%, <1–2%
and <1% of total energy intake, respectively. Reducing
the intake of SFA (which are known to raise total and
low-density lipoprotein (LDL) cholesterol) and increasing
the intake of n 3 PUFA is particularly encouraged.
Among the n 3 PUFA, eicosapentaenoic acid (EPA,
20:5n 3) and docasahexaenoic acid (DHA; 22:6n 3)
have been demonstrated to have important roles in reducing the risk of cardiovascular disease, are critical for proper
brain and visual development in the foetus, the maintenance of neural and visual tissues throughout life (Calder,
2004; Leaf, Xiao, Kang, & Billamn, 2003) and may have
N. Scollan et al. / Meat Science 74 (2006) 17–33
roles in reducing cancer and obesity/type-2 diabetes
(WHO, 2003). Meat, fish, fish oils and eggs are important
sources of these n 3 PUFA for man. However, the
opportunity for increased intake of long chain n 3 PUFA
from fish and fish oils appears limited due to low consumption of fish and concerns over the future sustainability of
this source (Williams & Burdge, 2006). This has resulted
in increased attention being devoted to increasing these
fatty acids in other important food sources. Attention
has also focused on the extent to which consumption of
the precursor of the n 3 series, a-linolenic acid can provide sufficient amounts of tissue EPA and DHA through
the n 3 PUFA elongation–desaturation pathway (Williams & Burdge, 2006).
Beef and other ruminant products such as milk are dietary sources of conjugated linoleic acid (CLA; Ritzenthaler
et al., 2001). The dominant CLA in beef is the cis-9, trans11 isomer, which has being identified as possessing a range
of health promoting biological properties including antitumoral and anticarcinogenic activities (De la Torre, Debiton
et al., 2006).
Due to the above, considerable attention has been
placed on improving the nutritional value of beef and
the development of products which are beneficial to
human health and disease prevention. While protein content and amino acid profiles are little influenced by animal
production factors such as nutrition and genetics, it is
recognised that micronutrient content, fat content and
fatty acid composition may be altered. Most attention
has been devoted to lipid composition. Hence, this paper
is primarily concerned with progress on altering the fatty
acid composition of beef, including its relationship to some
components of meat quality such as colour shelf life and
sensory attributes. Emphasis is placed on intramuscular
fat (IMF), including a review of genetic and nutritional
factors influencing the amount and fatty acid composition
of IMF.
2. Fat content and fatty acid composition of beef
Fat in beef is present as membrane fat (as phospholipid),
intermuscular fat (between the muscles), IMF and subcutaneous fat. Fat content varies widely depending on the cut
and degree of trimming. Lean beef has a low IMF content,
typically 2–5% and in many countries this is accepted as
being ‘‘low in fat’’. Marbling fat is an important meat quality trait in relation to juiciness, aroma and tenderness and
is the fat depot of most interest in relation to fatty acid
composition and human health. It refers to the white flecks
or streaks of adipose tissue between the bundles of muscle
fibres. It is thus closely linked to IMF content. In continental Europe, IMF content in beef is low, but still higher than
that in poultry and pork, but this very much depends upon
muscle and genotype. Modern European broilers may have
5% fat in the thigh meat but <1% in the skin-off breast
meat. Flavour score markedly increases with increasing
IMF content above 4–5% (Goutefongea & Valin, 1978).
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If tenderness is controlled, flavour and juiciness scores
show curvilinear positive relationships with IMF content
up to 14–20% (Thompson, 2004). These relationships along
with the interest in the fatty acid composition of IMF have
increased the awareness of producers in altering the
amount and composition of this fat depot in beef.
2.1. Fatty acid profile of IMF and relationships to human
health
Intramuscular fat consists on average, of 0.45–0.48,
0.35–0.45 and up to 0.05 of total fatty acids as SFA, monounsaturated fatty acids (MUFA) and PUFA, respectively.
The PUFA:SFA (P:S, taken as (18:2 + 18:3)/(14:0 +
16:0 + 18:0)) ratio for beef is typically low at around 0.1
(Choi, Enser, Wood, & Scollan, 2000; Scollan et al.,
2001), except for double muscled animals which are very
lean (<1% IMF) where P:S ratios are typically 0.5–0.7
(Raes, De Smet, & Demeyer, 2001). The n 6:n 3 ratio
for beef is beneficially low, typically less than 3, reflecting
the considerable amounts of beneficial n 3 PUFA in beef,
particularly 18:3n 3 and the long chain PUFA, EPA and
DHA.
The predominant SFA are 14:0 (myristic acid), 16:0
(palmitic acid) and 18:0 (stearic acid), the latter representing 0.3 of total SFA. SFA influence plasma cholesterol,
though 18:0 is regarded as neutral in this regard (Yu, Derr,
Etherton, & Kris-Etherton, 1995) and 16:0 is less potent
than 14:0 (Williamson et al., 2005). Linoleic and a-linolenic
acids are the main PUFA while oleic acid (18:1n 9) is the
most prominent MUFA, with the remainder of the MUFA
occurring mainly as cis and trans isomers of 18:1. The
PUFA and MUFA are generally regarded as beneficial
for human health and there is evidence of beneficial effects
of trans-vaccenic acid (TVA). Rats given supplements of
CLA cis-9, trans-11 would indicate that TVA (the precursor of CLA in tissue and which is the major trans fatty acid
in beef) could also add to the beneficial effects of CLA
cis-9, trans-11 on cancer (Corl, Barbano, Bauman, & Ip,
2003) and atherogenesis (Lock, Horne, Baumann, & Salter,
2005; Valeille et al., 2005). Beef also contains small
amounts of the long chain C20/22 PUFA, EPA and DHA
and recent research has demonstrated that red meat is an
important source of these fatty acids for man (Howe,
Meyer, Record, & Baghurst, 2006).
Dannenberger et al. (2004) reported 10 isomers of CLA
in beef with CLA cis-9, trans-11 representing approximately 70% of total CLA isomers. Biological effects have
been widely investigated for two of these isomers. The
anticarcinogenic and antiatherogenic effects of cis-9,
trans-11 and the anti-obesity effects of trans-10, cis-12
have been well documented (Belury, 2003). It is evident
from this discussion that different fatty acids have different effects on health and disease prevention and this has
placed more attention on beneficially altering the fatty
acid profile of a particular food and not simply its fat
content.
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N. Scollan et al. / Meat Science 74 (2006) 17–33
Intramuscular fat mainly consists of triacylglycerols and
phospholipids. The triacylglycerols serve as a concentrated
source of energy for the body and are deposited in adipocytes. The total IMF content generally depends on the
amount of triacylglycerols, whereas the amount of
phospholipid, as the building blocks of cell membranes, is
relatively constant. Hence there is a strong relationship
between IMF and the content of triacylglycerols which is
mainly dependent on the degree of overall body fatness,
breed and muscle type. The SFA 16:0 and 18:0 and the
MUFA 18:1n 9 account for approximately 0.8 of total
triacylglycerol fatty acids. The dominant PUFA are
18:2n 6 and 18:3n 3 representing approximately 0.02
of total triacylglycerol fatty acids. In ruminants, the fatty
acids in triacylglycerols are influenced by diet but to a
much lesser extent than in monogastrics due to biohydrogenation of dietary fatty acids in the rumen. In phospholipid the proportion of PUFA is much higher than in
triacylglycerols, containing not only the essential fatty
acids 18:2n 6 and 18:3n 3 but also their longer chain
derivatives such arachidonic acid (20:4n 6), EPA, DPA
and DHA. Dannenberger et al. (2004) reported that the
proportion of PUFA in muscle phospholipids of German
Holstein bulls at 630 kg live weight was 0.37–0.41 relative
to 0.02 in the triacylglycerols. The phospholipids play central roles in cell membrane function and the PUFA composition is strictly controlled by a complex enzymatic system
responsible for the conversion of 18:2n 6 and 18:3n 3
to their longer chain derivatives (Raes, De Smet, &
Demeyer, 2004). The phospholipid fatty acids are less influenced by diet, but differences in the content of n 6 and
n 3 long chain PUFA do occur. For example, pasture
feeding caused an accumulation of the n 3 fatty acids
in phospholipids and triacylglycerols compared to concentrate feeding (Dannenberger et al., 2004; see subsequent
sections). Before considering further the relationships
between nutrition and fatty acid composition of IMF, it
is appropriate to provide an overview of the physiological
regulation of IMF deposition.
2.2. Regulation of IMF deposition
Intramuscular fat is stored to a major extent within the
intramuscular adipocytes. Marbling fat is indeed a true adipose tissue embedded within a connective tissue matrix in
close proximity to a blood capillary network. Therefore,
the number and the diameter of intramuscular adipocytes
may be good predictors of marbling (Cianzo, Topel,
Whitehurst, Beitz, & Self, 1985).
The number of preadipocytes in the muscle, which ultimately differentiate into intramuscular adipocytes, depends
on stem or progenitor cells (Harper & Pethick, 2004). The
different lineages to derive adipose, muscle and fibroblastic
cells remain however largely unknown. Alteration in cell
cycling, preferential clonal selection of some specific progenitor populations, differential proliferation of different
stem cells and/or interactions between (pre)adipocytes
and myoblasts may control the relative proportions of
the different cell types present in the muscle tissue. For
instance, myostatin promotes the differentiation of multipotent mesenchymal cells into the adipogenic lineage and
inhibits myogenesis (Artaza et al., 2005).
IMF also results from the balance between uptake, synthesis and degradation of triacylglycerols. Therefore, many
metabolic pathways (fat uptake from blood, de novo fatty
acid synthesis, mitochondrial activity, etc.) in both adipocytes and myofibres could contribute to the variability of
IMF content (Hocquette, Ortigues-Marty, Pethick, Herpin, & Fernandez, 1998). In fact, IMF content results from
a balance between synthesis and degradation of fats within
muscles, rather than from one specific energy metabolic
pathway (Gondret, Hocquette, & Herpin, 2004). This is
probably the reason why muscles which have a great ability
to deposit fat are in fact oxidative muscles (rich in mitochondria and with a high fat turnover) (Hocquette et al.,
2003).
In practice, it is clear that the development of IMF content or marbling score is late maturing. More precisely, it is
due to maintained or increased fat synthesis in combination with declining muscle growth as animals get older
(Pethick, Harper, & Oddy, 2004). The IMF content at birth
or at the beginning of the finishing period is likely to be
mainly explained by the number of preadipocytes which
depends itself on genetic and nutritional factors. For
instance, late-maturing beef breeds (Belgian blue, Limousin
and Blonde d’Aquitaine) deposit more muscle and less fat
compared to dairy breeds or early-maturing beef breeds
(Angus and Japanese Black cattle). The major nutritional
and/or management tool for increasing the development
of marbling is to maximise the availability of net energy
(and glucose) for fat synthesis during finishing (Harper &
Pethick, 2004). This is the reason why the IMF content is
lower for pasture than for grain finishing. At the cellular
level, this may be due to increased levels of anabolic hormones (insulin) which stimulates lipogenesis and/or to a
preference of marbling adipocytes for carbohydrate carbon
to synthesise fatty acids unlike adipocytes of the carcass
(Pethick et al., 2004).
2.3. Genetic control of IMF accumulation
Marbling and IMF content have much higher genetic
variability (h2 = 0.35–0.50) than tenderness, flavour or juiciness scores (see reviews of Burrow, Moore, Johnston,
Barense, & Bindon, 2001; Hocquette, Renand, Levéziel,
Picard, & Cassar-Malek, 2005), and whilst IMF content
is often positively correlated to tenderness, especially when
large numbers of animals are studied (Thompson, 2004),
the relationships are usually weak. Selection on marbling
score (highly correlated with IMF content) may improve
tenderness, but as marbling is positively correlated to carcass fatness, selection on IMF or marbling will have undesirable effects on carcass composition. Genetic selection in
favour of leaner carcasses decreased IMF content and also
N. Scollan et al. / Meat Science 74 (2006) 17–33
3. Strategies influencing the fatty acid composition of beef
Genetic and nutritional approaches have been widely
studied in relation to fatty acid composition of beef,
although it is acknowledged that genetic factors generally
provide smaller differences than dietary factors (see De
Smet, Raes, & Demeyer, 2004 for review). Nevertheless,
as concluded by De Smet et al. (2004), even though breed
differences are generally small they do reflect differences
in underlying gene expression or enzymes involved in fatty
acid synthesis (as discussed above), and therefore warrant
consideration. Taniguchi, Mannen et al. (2004) reported
that stearoyl CoA desaturase (delta-9-desaturase) mRNA
expression level was related to MUFA percentage in Holstein Japanese Black cattle and describe a SNP in Japanese
Black cattle which contributed to higher MUFA percentage and lower melting point in IMF (Taniguchi, Utsugi
et al., 2004).
Of particular note is the association between fatness and
P:S ratio (Fig. 1). As the content of SFA and MUFA
increases faster with increasing fatness than does the con-
tent of PUFA, the relative proportion of PUFA and the
P:S ratio decrease with increasing fatness. Hence the low
fat content (<1%) explains the beneficially high P:S ratio
(0.5–0.6) in the double-muscled Belgian Blue bulls (Raes
et al., 2001). In contrast the n 6:n 3 ratio in meat of
double-muscled Belgian Blue bulls is high (5–6), but may be
improved by using the nutritional approaches outlined
below (Raes, De Smet, Balcaen, Claeys, & Demeyer, 2003,
2004).
3.1. Forages and the fatty acid composition of beef
Plants are the primary source of n 3 PUFA, both in
the terrestrial and marine ecosystems. Plants have the
unique ability to synthesise de novo 18:3n 3 which is
the building block of the n 3 series of essential fatty acids
and elongation and desaturation of this fatty acid results in
the synthesis of EPA and DHA. The formation of these
long chain n 3 PUFA by marine algae and their transfer
through the food chain to fish, accounts for the high
amounts of these important fatty acids in fish oils (see subsequent section).
Forages such as grass and clover contain a high proportion (50–75%) of total fatty acids as a-linolenic acid (Dewhurst, Shingfield, Lee, & Scollan, in press). Exploiting the
potential of herbage as an alternative to marine sources
of PUFA is an important nutritional strategy for enhancing the content of n 3 PUFA in beef. The transfer of
18:3n 3 from forage through meat is dependent on two
important processes, (1) increasing the level of 18:3n 3
in the forage (and hence into the animal) and (2) reducing
the extent of ruminal biohydrogenation. These factors have
recently been reviewed by Palmquist et al. (2005) and Dewhurst et al. (in press) and will not be considered further
here.
Feeding fresh grass or grass silage compared to concentrates, rich in 18:3n 3 and 18:2n 6, respectively, results
in higher concentrations of n 3 PUFA in muscle lipids,
both in the triacylglycerol and phospholipid fractions
(Tables 1(i) and 2; Nuernberg, Dannenberger et al., 2005;
0.9
Control
PLS1
PLS2
0.8
0.7
P:S ratio
induced a lower activity level of some mitochondrial
enzymes especially in oxidative muscles. A positive correlation between IMF content and a marker of adipocyte differentiation (the expression of the A-FABP gene) has
been shown among animals (Hocquette et al., 2004).
As reviewed by Kühn et al. (2005), several QTL and
genetic markers for marbling were reported from experiments performed in North America or in Australia under
feedlot production conditions. The markers include polymorphisms of the thyroglobulin gene (precursor of thyroid
hormones), of microsatellite loci CSSM34 and ETH10, of
the DGAT1 gene encoding diacylglycerol-O-acyltransferase
(involved in the last stages of fat synthesis) and of the retinoid related orphan receptor C (gamma) (RORC). Mutation in GDF8 (myostatin) not only decreases IMF content
but also increases muscle mass underlying the relationships
between muscle and IMF development (Harper & Pethick,
2004). Research programmes (such as the EU-funded project GeMQual, www.gemqual.org) are currently in progress
for the identification of single nucleotide polymorphisms
(SNP) in a large set of candidate genes with the objective
of being able to evaluate their association with meat quality
variables (including IMF content). Finally, the advent of
genomics has great potential to discover new molecular
markers. It has for instance confirmed the importance of
A-FABP for IMF deposition (Wang et al., 2005) and the
orientation towards fast glycolytic type muscles in double
muscled cattle (which produce lean beef) (Bouley et al.,
2005), but has also provided evidence for new genes associated with high muscle growth potential and/or less IMF
(Bouley et al., 2005; Sudre et al., 2005). Thus, genomics
is likely to provide future opportunities, as well as new
challenges, in the quest for achieving marbling performance and later will provide knowledge on the control of
muscle fatty acid composition.
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0.6
0.5
0.4
0.3
0.2
0.1
0
0
2000
4000
6000
8000
10000
Total fatty acids (mg/100 g muscle)
12000
Fig. 1. Relationship between P:S ratio and total fatty acid content of beef
longissimus muscle (control, PLS1 and PLS2 refer to 0, 500, 1000 g/d
protected lipid supplement; Scollan et al. (2003)).
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N. Scollan et al. / Meat Science 74 (2006) 17–33
Warren, Scollan, Hallett, Enser, & Richardson, 2002). Significantly, grass compared to concentrate feeding not only
increased 18:3n 3 in muscle phospholipid but also EPA,
DPA and DHA (see Table 2; Dannenberger et al., 2004;
Warren et al., 2002). In comparison, concentrates rich in
18:2n 6 lead to higher concentrations of 18:2n 6 and
associated longer chain derivatives (20:4n 6). Studies in
Ireland showed that both the proportion of grass in the diet
(Table 1(ii); French et al., 2000) and length of time on grass
(Table 1(iii) Noci, Monahan, French, & Moloney, 2005)
were important in determining the response in beef fatty
acids. French et al. (2000) also found significant reductions
in the proportion of SFA, both 16:0 and 18:0 with grass
feeding, Collectively these responses in both SFA and
n 3 PUFA contribute towards beneficial changes in P:S
(increasing) and n 6:n 3 ratios (decreasing). The recent
report by Razminowicz, Kreuzer, and Scheeder (2006) confirmed these grass forage/pasture effects in retail beef. They
noted that pasture beef relative to ‘‘conventional’’ beef or
intensively produced young bulls had higher amounts of
n 3 PUFA and resulted in an n 6:n 3 ratio consistently below 2. Feeding steers indoors on maize silage
and concentrate resulted in higher concentrations of
18:2n 6 (and less 18:3n 3) and a less favourable
n 6:n 3 ratio than pasture-finished steers (Varela
et al., 2004).
Feeding mixtures of grass and red clover relative to
grass alone increased the deposition of both n 6 and
n 3 PUFA in muscle of finishing beef steers, resulting
in increases in the P:S ratio (Table 1(iv); Scollan et al.,
Table 1
Influence of forage on the fatty acid composition (mg/100 g tissue) of beef longissimus muscle
(i) Grass v. concentrate (Adapted from Warren et al. (2003))
Fatty acids
Grass
Concentrate
SED
Significance*
Total
18:2n
18:3n
20:5n
22:5n
22:6n
n 6:n
P:S
1724
146.9
7.2
4.5
10.8
1.3
8.9
0.24
139.3
6.68
1.60
1.05
1.28
0.30
0.24
0.010
***
***
***
***
***
***
***
***
2581
62.0
32.0
17.7
10.8
5.0
1.2
0.09
6
3
3
3
3
3
(ii) Proportion of grass (g/kg DM) in the diet (Adapted from French et al. (2000))
Fatty acids
Total
18:2n
18:3n
20:5n
22:6n
n 6:n
P:S
6
3
3
3A
3
Grass (g/kg DM)
0
510
770
1000
3410
120.5
29.3
4.9
–
4.15
0.09
4490
105.8
35.4
11.0
–
2.86
0.10
4020
94.4
41.1
9.8
–
2.47
0.11
4360
85.9
46.0
9.4
–
2.33
0.13
SED
Significance
650.5
6.05
1.78
1.32
NS
**(linear)
**(linear)
*(quadratic)
0.197
0.010
**(linear)
**(linear)
(iii) Length of grass feeding (days) (Adapted from Noci, Monahan, et al. (2005))
Fatty acids
0
40
99
158
SED
Significance
Total
18:2n
18:3n
20:5n
22:6n
n 6:n
P:S
2754
59.4
30.9
6.4
2.78
1.63
0.12
2515
59.0
34.4
7.7
2.72
1.46
0.15
177.5
3.32
1.86
0.50
0.606
0.108
0.009
NS
NS
***
***
NS
***
***
(iv) Grass v. red clover (Adapted from Scollan et al. (2006))
Fatty acids
Grass silage
50:50 mix grass/red clover
Red clover
Red clover + vitamin E
SED
Significance
Total
18:2n
18:3n
20:5n
22:5n
22:6n
n 6:n
P:S
4001
113.2c
50.7c
14.9
25.11
2.78
2.30a
0.10b,c
3074
99.3b
37.5b
14.5
24.25
2.65
2.66b
0.12c
604.7
6.68
3.83
1.33
2.93
0.275
0.15
0.01
NS
***
***
NS
NS
NS
***
**
*
A
6
3
3
3
3
6
3
3
3
3
3
2461
62.1
19.6
5.6
3.22
2.21
0.12
3081
73.2a
22.5a
12.9
21.65
2.51
3.28c
0.07b
2329
63.7
25.4
5.5
2.86
1.99
0.14
3639
92.8b
34.1b
13.4
23.89
2.34
2.73b
0.09a,b
In this and other tables NS = not significant; *P < 0.05; **P < 0.01; ***P < 0.001.
Not identified on chromatogram.
(linear)
(linear)
(linear)
(linear)
N. Scollan et al. / Meat Science 74 (2006) 17–33
Table 2
Influence of concentrate or grass silage on fatty acid composition
(proportion · 100) of the phospholipid fraction of beef longissimus muscle
(Warren et al., 2002)
18:2n
18:3n
20:3n
20:4n
20:5n
22:5n
22:6n
6
3
6
6
3 EPA
3 DPA
3 DHA
Concentrate
Grass silage
SED
Significance
23.3
0.8
2.7
10.5
0.8
2.1
0.2
8.7
3.7
1.2
6.3
3.4
4.6
0.9
0.36
0.05
0.06
0.17
0.06
0.09
0.04
***
***
***
***
***
***
***
2006). Companion studies have revealed that the red clover
response is related to reductions in ruminal biohydrogenation of PUFA, which is possibly related to the protective
effects of the enzyme polyphenol oxidase (PPO; Lee
et al., 2004). Studies in milk have revealed that Alpine pasture results in a higher content of 18:3n 3 than lowland
pasture, as a result of reduced ruminal biohydrogenation
of dietary 18:3n 3 (Leiber, Kreuzer, Nigg, Wettstein, &
Scheeder, 2005). Norwegian sheep finished on mountain
pastures had 25% more PUFA than similar sheep raised
on improved lowland pastures (Adnoy et al., 2005). Similar
results are not available for beef, but identification of the
‘‘Alpine factor’’ responsible for the reduction in biohydrogenation should be pursued.
3.2. Supplementary lipids and the fatty acid composition of
beef
3.2.1. Unprotected lipids
The main sources of supplementary fatty acids in ruminant rations are plant oils and oilseeds, fish oil, marine
algae and fat supplements (Givens et al., 2000). Since dietary inclusion of fatty acids must be restricted (to 60 g/kg
dry matter consumed, approx.) to avoid impairment of
rumen function, the capacity to manipulate the fatty acid
composition by use of ruminally-available fatty acids is
limited. Despite ruminal biohydrogenation, a proportion
of dietary PUFA bypasses the rumen intact and is
absorbed and deposited in body fat (Wood & Enser,
1997). Thus, linseed or linseed oil (rich in 18:3n 3) can
increase the concentration of 18:3n 3 in tissue with an
associated desirable decrease in the n 6: n 3 PUFA
ratio (Scollan et al., 2001, Table 3(i)). Similarly, sunflower
seed or sunflower oil (rich in 18:2n 6) can increase the
concentration of 18:2n 6 in tissue but with an associated
undesirable increase in the n 6: n 3 PUFA ratio (Garcia, Amstalden, Morrison, Keisler, & Williams, 2003; Noci,
O’Kiely, Monahan, Stanton, & Moloney, 2005). Dietary
inclusion of 18:3n 3 generally also increases the concentration of EPA but not DHA in tissue (Scollan et al.,
2001). The potential of fish oil (rich in both the long-chain
n 3 PUFA) to increase their concentration in beef is illustrated in Table 3 (Scollan et al., 2001) and the increase is
dependant on the level of dietary inclusion (Noci, Mona-
23
han, Scollan, & Moloney, 2006). While the supplementation strategies described above can cause sizeable changes
in the n 6:n 3 PUFA ratio they generally do not
increase the P:S ratio in the meat above the 0.1–0.15 normally observed.
3.2.2. Protected lipids
Durand, Scislowski, Gruffat, Chillard, and Bauchart
(2005) demonstrated the potential to markedly increase
the concentration of n 3 PUFA in beef muscle by infusing 18:3n 3 (as linseed oil) directly into the small intestine. Thus, infusing an amount of linseed oil similar to
that consumed, increased the concentration of 18:3n 3
in total lipid from 26.3 to 176.5 mg/100 g muscle. Infusion
also resulted in a high P:S ratio (0.495 relative to the recommended target of >0.4) and low n 6:n 3 ratio (1.04
relative to the recommended target of <2–3). For practical
exploitation of the capacity of muscle to deposit n 3
PUFA, methods to protect dietary lipids from ruminal degradation are under on-going investigation. A variety of
procedures have been explored including the use of intact
oilseeds, heat/chemical treatment of intact/processed oilseeds, chemical treatment of oils to form calcium soaps
or amides, emulsification/encapsulation of oils with protein
and subsequent chemical protection (see Ashes, Gulati,
Kitessa, Fleck, & Scott, 2000; Gulati, Garg, & Scott,
2005). Using the latter technology, Scollan, Enser, Gulati,
Richardson, and Wood (2003) showed that a protected
plant oil supplement (with n 6:n 3 PUFA ratio of
2.4:1) markedly improved the P:S ratio (from 0.08 to
0.27) but increased the n 6:n 3 PUFA (from 2.75 to
3.59) in muscle. It is interesting that in this study the
increase in P:S was associated with an increase in PUFA
content but also a reduction in IMF (as discussed above;
Fig. 1). In a subsequent study, a protected plant oil supplement with n 6:n 3 PUFA ratio of 1:1 decreased the
n 6:n 3 PUFA ratio in muscle (from 3.59 to 1.88) while
maintaining the high P:S ratio (Scollan, Enser, Richardson,
Gulati, Hallett, Nute et al., 2004, Table 3(ii)). No effect was
observed on the concentration of DHA in either study.
Ruminal protection of fish oil however, increased the concentration of EPA and DHA in tissue but had little effect
on the P:S ratio and improved the n 6:n 3 PUFA ratio
only at the highest level fed (Richardson, Hallett et al.,
2004, Table 3(iii)). This may reflect the inclusion of 100 g
unprotected fish oil in all treatments. As discussed previously, the long-chain n 3 PUFA are incorporated mainly
into membrane phospholipids and are not incorporated
into triacylglycerols to any important extent in ruminants.
This provides the opportunity to manipulate intramuscular
fatty acid composition of ruminant meat without large
increases in fatness per se. Since the concentrations of
EPA and DHA in fish oil are dependent on the species of
fish and represent, at most, 25% of fish oil fatty acids, often
the rest being rich in SFA (Givens et al., 2000), a prudent
future strategy would be to concentrate these fatty acids
prior to ruminal protection. Moreover, since the most
24
N. Scollan et al. / Meat Science 74 (2006) 17–33
Table 3
Influence of fat sources on the fatty acid composition (mg/100 g tissue) of beef longissimus muscle
(i) Different sources of oil (Adapted from Scollan et al. (2001))
Fatty acids
Control
Linseed
Fish oil
Linseed/fish oil
SED
Significance
Total
18:2n
18:3n
20:5n
22:5n
22:6n
n 6:n
P:S
4292
66
26a
23c
16
4.6b
0.91b
0.05
3973
64
30a
15a,b
16
4.9b
1.11b
0.05
741.0
9.2
5.6
1.9
0.7
0.52
0.106
0.008
NS
NS
**
***
NS
***
**
NS
6
3
3
3
3
3
3529
81
22a
11a
15
2.2a
2.00a
0.07
4222
78
43b
16b
15
2.4a
1.19a
0.07
(ii) Plant oils protected from ruminal biohydrogenation (Adapted from Scollan, Enser, Richardson, Gulati, Hallett, Wood et al. (2004))
Control
Total
18:2n
18:3n
20:5n
22:5n
22:6n
n 6:n
P:S
6
3
3
3
3
3
4685
120
29a
13a
23a,b
1.9
2.27c
0.07a
PLSA (g/d)
400
800
1000
4976
255
102b
15a
24b
1.8
2.02b
0.18b
4880
279
118b,c
14a
20a
1.5
2.00b
0.20b
4895
305
139c
16a
20a
1.6
1.88a
0.22b
SED
Significance
737.0
23.4
13.1
1.1
1.7
0.272
0.055
0.018
NS
***
***
*
*
NS
***
***
SED
Significance
614.2
6.7
1.9
1.6
1.2
0.81
0.060
0.007
NS
NS
NS
*
*
***
*
NS
(iii) Fish oil protected from ruminal biohydrogenation (Richardson, Hallett et al., 2004)
Control
Total
18:2n
18:3n
20:5n
22:5n
22:6n
n 6:n
P:S
A
B
6
3
3
3
3
3
4698
88
25
14a
23b
3.4a
1.70b
0.06
PFOB (g/d)
50
100
200
4092
81
23
14a
21a,b
7.0b
1.55a
0.06
3858
87
23
15a,b
20a
9.8c
1.61a
0.07
4258
93
26
18b
19a
12.0d
1.56a
0.07
PLS = protected lipid supplement.
PFO = protected fish oil.
effective protection strategies to date have been on a noncommercial scale and involved formaldehyde, the use of
which may not be permitted by some regulatory authorities, development of alternative protection technologies is
needed. The recent report on the efficacy of a whey protein
gel complex to ruminally protect PUFA is encouraging in
this regard (Carroll, DePeters, & Rosenberg, 2006).
3.3. Dietary effects on trans fatty acids in beef
Human metabolic studies have shown that trans fatty
acids and SFA like lauric acid, myristic acid and palmitic
acid elevate LDL cholesterol (Li, Siramornpun, Wahlquist,
Mann, & Sinclair, 2005). In response to concerns about the
consumption of trans fatty acids and potential impact on
health, the US Dietary Guidelines Committee concluded
that the intake of trans fatty acids should be below 1% of
energy (Willet, 2005). In Canada and the US it is mandatory to declare the trans fatty acid content of food from
January 2006. Evidence is accumulating that different trans
18:1 isomers have differential effects on plasma LDL cho-
lesterol and this is an area of active investigation (Willet,
2005). For example, there is support that trans-9 and
trans-10 18:1 are more powerful in increasing plasma
LDL cholesterol than trans-11 18:1 (Willet, 2005). It is also
recognised that trans vaccenic acid (trans-11 18:1, TVA) is
the precursor for tissue synthesis of beneficial CLA (CLA
cis-9, trans-11) in both man and in animals.
Important differences exist in the profile of trans fatty
acids of different foods and attention has been given to that
of partially hydrogenated vegetable oils compared to that
of ruminant fats. Industrial hydrogenation results in a wide
range of equally distributed isomers relative to IMF in beef
(Fig. 2). The daily consumption of trans fatty acids from
industrially hydrogenated fat is up to ten times higher than
that from ruminant fat (Stender & Dyerberg, 2003).
TVA is the most abundant trans 18:1 isomer in beef and
lamb (Dannenberger et al., 2004; Nuernberg, Nuernberg
et al., 2005, Fig. 2). The intramuscular lipids of bulls contain approximately 2.8–3.2% of total trans 18:1 isomers
(Nuernberg et al., 2005). As reflected in Fig. 2, pasture
feeding increased the relative proportion of TVA in muscle
N. Scollan et al. / Meat Science 74 (2006) 17–33
on two isomers: CLA cis-9, trans-11 and CLA trans-10,
cis-12 (Belury, 2003; Kritchevsky, 2003; Pariza et al.,
2001). Studies on pure single isomers showed that they
have differences in biological activities as reported in recent
reviews by Banni, Heys, and Wahle (2003), Khanal (2004)
and Martin and Valeille (2002).
CLA cis-9, trans-11 is the major CLA isomer in ruminant milk and meat products and is mainly deposited in
the triacylglycerols (Dannenberger et al., 2004). CLA cis-9,
trans-11 is formed during biohydrogenation of linoleic acid
in the rumen and it was initially assumed that this was the
source of CLA cis-9, trans-11 in milk and intramuscular fat
(Harfoot & Hazelwood, 1998). However, Griinari et al.
(2000) and Palmquist (2001) showed that the primary
source of CLA cis-9, trans-11 is endogenous synthesis from
TVA formed during ruminal biohydrogenation and involving D9-desaturase (Khanal & Dhiman, 2004; Song &
Kennelly, 2003). There appears to be a linear relationship
between muscle TVA and CLA content (Enser et al.,
1999). The CLA content can be increased by different
of bulls and lambs. Avoiding increases in trans isomers
when attempting to decrease SFA and/or enhance PUFA
is important. In this respect, it is important to note that
grass and pasture based approaches result in lower effects
on trans-fatty acids relative to supplementation with plant
oils or fish oils (Noci, O’Kiely, et al., 2005; Noci et al.,
2006; Scollan et al., 2001).
3.4. Dietary effects on CLA in beef
(%)
Conjugated linoleic acids consist of a collection of positional and geometric isomers of octadecadienoic acid.
Ruminant meats and milk and their products are the main
natural source of CLA in the human diet. CLA has been
linked to a multitude of potential health benefits, including
inhibition of carcinogenesis, reduced rate of fat deposition,
altered immune response, reduced serum lipids, antidiabetic and antiatherogenic effects (Bauman, Baumgard,
Corl, & Griinari, 1999; Belury, 2003; Kritchevsky, 2003;
Pariza, Park, & Cook, 2001). Most research has focused
45
40
35
30
25
20
15
10
5
0
25
42.2
Concentrate
(Beef muscle)
15.2
14.05
0.334
0.32
1.78
4
5
6-8*
12.4
4.8
9
10
11
12
13/14
4.8
5.2
15
16
6.9
7.5
15
16
3
2.3
15
16
60
50
(%)
40
49.4
Pasture
(Beef muscle)
30
17.6
20
10
10.2
0.28
0.24
1.03
4
5
6-8*
3.02
3.8
9
10
0
25
Hydrogenated oil§
20
12
13/14
14
13.6
20.3
17.3
14.7
(%)
21.7
11
15
10
5
0.2
0.2
4
5
0
6-8*
9
10
11
12
13/14
Double bond position (18:1 trans )
Fig. 2. Distribution of trans 18:1 isomers in ruminant fat and industrially hydrogenated vegetable oil (§Stender and Dyerberg (2003) and Dannenberger
et al. (2004)).
26
N. Scollan et al. / Meat Science 74 (2006) 17–33
dietary strategies (De La Torre et al., 2006; Schmid et al.,
2006). Diets containing a proportionally high level of linolenic acid in the fat, such as fresh grass, grass silage, and
pasture feeding during the finishing periods, resulted in
increased deposition of CLA cis-9, trans-11 in muscle
(Enser et al., 1999; French, O’Riordan, Monahan, Caffrey,
& Moloney, 2003; Scollan et al., 2001; Shanta, Moody, &
Tabeidi, 1997). French et al. (2003) reported a significant
increase in CLA cis-9, trans-11 in muscle of crossbred
steers grazed for 85 days on pasture compared to concentrate, averaging 1.08% and 0.37% of total fatty acids,
respectively. Dhiman (2001) and Poulson et al. (2001)
observed a significant increase in CLA cis-9, trans-11 in
muscle of crossbred steers on forage and pasture without
grain supplementation. Similarly, Steen and Porter (2003)
reported that the content of CLA cis-9, trans-11 in muscle
and subcutaneous fat from steers finished on pasture was
three times higher than that from steers finished on concentrate. Nuernberg et al. (2005) reported, that pasture feeding
resulted in a significant increase of CLA cis-9, trans-11
from 0.50% to 0.75% in muscle lipids of German Holstein
and German Simmental bulls compared with concentratefed bulls. Furthermore, adding oil seeds, vegetable oils
and fish oil to the diet have proved to be efficient strategies
to increase the CLA content in muscle lipids (Schmid, Collomb, Sieber, & Bee, 2006). The authors reviewed the available data on intramuscular CLA content in meat and meat
products originating from different animal species. However, the amount of CLA found in meat is small, relative
to the recommended daily intake for health benefits in
human, which is 3500 mg/d (Ha, Grimm, & Pariza,
1989). It is important to consider the net CLA yield to
the consumer rather than only the concentration in the dietary lipid. Values for CLA cis-9, trans-11 concentrations
(mg/100 g fresh muscle) in beef are sparse in the literature
and a selection is summarised in Table 4. Certain breeds of
cattle that have a tendency to deposit high amounts of IMF
in muscle (i.e. Wagyu or Wagyu · Limousin steers) will
deliver a greater amount of CLA cis-9, trans-11 to the consumer (Table 4; note the data in this Table does not take
into account conversion of TVA to CLA in human tissue).
Bauchart, Gladine, Gruffat, Leloutre, and Durand (2005)
and De La Torre, Gruffat et al. (2006) have shown that
not only does lipid supplementation affect the proportion
of CLA produced, but this also depends upon basal diet,
breed, age and sex of the animals.
Furthermore, there are only a few publications dealing
with the CLA isomer distribution in different beef tissues
using silver-ion HPLC (Ag+-HPLC). This is particularly
important because the individual CLA isomers show different biological activities (Banni et al., 2003; Pariza et al.,
2001; Khanal, 2004). Additionally, the distribution pattern
in the tissue lipids will be affected by the composition of the
ration consumed (Dannenberger et al., 2004; Dannenberger et al., 2005; De La Torre, Gruffat et al., 2006; Nuernberg et al., 2002; Table 5). There is a lack of information
on the metabolic pathways of individual trans 18:1-isomers
and CLA isomers in muscle and their different biological
activities and further research is needed.
4. Fatty acids and meat quality
4.1. Meat flavour
The flavour of red meats is derived from the Maillard
reaction between amino acids and reducing sugars and the
thermal degradation of lipid. The former produces
roasted/meaty flavours and the latter the species differences
in flavour (Gandemer, 1999; Mottram, 1998). Strategies
which alter the fatty acid composition of the lipid fraction
of meat could also alter the amount and type of volatiles
produced and hence its aroma and flavour (Elmore, Mottram, Enser, & Wood, 1999; Elmore et al., 2004). In a study
comparing grass- and concentrate-finished animals, the
concentrate-fed animals had higher concentrations of linoleic acid in their meat and on cooking produced seven compounds at over three times the level found in meat from
grass-fed animals, which had much higher concentrations
of 18:3n 3 and produced a higher amount of only two
compounds, phyt-1-ene (10-fold) and phyt-2-ene (threefold), derivatives of chlorophyll (Elmore et al., 2004). These
are similar results to those of Larick et al. (1987) who found
that phy-2-ene, produced from cooking subcutaneous fat,
was a good marker of forage feeding and that nine other
compounds were useful in a discriminant analysis to predict
the length of time an animal had been fed on grass or grain.
Lorenz et al. (2002) quantified meat odour volatiles formed
after pressure-cooking meat from cattle fed forage or con-
Table 4
Concentration of CLA cis-9, trans-11 (mg/100 g fresh muscle) in longissimus muscle of different beef genotypes
Breed
Diet
CLA cis-9, trans-11
References
Wagyu, steers
Wagyu · Limousin, steers
Limousin, steers
Charolais, steers
Crossbred steers
German Holstein, bulls
German Simmental, bulls
Double-muscled Belgian Blue, bulls
Double-muscled Belgian Blue, bulls
Sunflower oil
Sunflower oil
Sunflower oil
Grass silage whole linseed
Grass silage
Pasture
Pasture
Crushed linseed
Extruded linseed
134
76
59
36
35
17
12
4.3
4.2
Mir et al. (2002)
Mir et al. (2004)
Mir et al. (2004)
Enser et al. (1999)
Steen and Porter (2003)
Dannenberger et al. (2005)
Dannenberger et al. (2005)
Raes et al. (2004)
Raes et al. (2004)
N. Scollan et al. / Meat Science 74 (2006) 17–33
27
Table 5
Concentration (mg/100 g fresh muscle) of CLA isomers in beef longissimus muscle lipids of beef (Dannenberger et al. (2005))
German Holstein
Concentrate
LSM
German Simmental
Pasture
SEM
n = 14
LSM
Concentrate
SEM
LSM
n = 14
Significance (P < 0.05)
Pasture
SEM
LSM
n = 13
SEM
n = 13
Intramuscular fat (%)
2.7
0.2
2.3
0.2
2.6
0.2
1.5
0.3
D
trans, trans
CLA trans-12, trans-14
CLA trans-11, trans-13
CLA trans-10, trans-12
CLA trans-9, trans-11
CLA trans-8, trans-10
CLA trans-7, trans-9
0.07
0.1
0.1
0.2
0.07
0.06
0.04
0.08
0.02
0.04
0.02
0.02
0.5
0.8
0.2
0.4
0.1
0.2
0.04
0.07
0.02
0.04
0.02
0.02
0.03
0.05
0.07
0.1
0.04
0.04
0.05
0.08
0.03
0.04
0.02
0.02
0.1
0.2
0.06
0.1
0.02
0.05
0.04
0.08
0.03
0.04
0.02
0.02
D,B,D*B
D,B,D*B
B
B,D*B
B
D,B,D*B
0.03
0.02
0.03
1.5
0.1
0.2
0.3
2.9
0.4
14.4
0.4
1.6
0.03
0.23
0.03
1.5
0.09
0.2
0.07
0.1
0.1
6.5
0.2
0.7
0.03
0.2
0.04
1.5
0.1
0.2
0.08
1.0
0.2
8.0
0.2
0.5
0.03
0.2
0.04
1.5
0.1
0.2
D,B,D*B
D,B,D*B
D,B
B
B
B
cis, trans; trans, cis
CLA cis-12, trans-14
CLA trans-11, cis-13
CLA trans-10, cis-12
CLA cis-9, trans-11
CLA trans-8, cis-10
CLA trans-7, cis-9
0.1
0.2
0.2
11.7
0.4
1.4
LSM is the least square means, SEM is the standard error of LSM.
D is the significant influence of diet, B is the significant influence of breed, D*B is the significant interaction of D*B.
centrate. ‘Green’ odour from meat of grass-fed animals was
connected with compounds (hexanals) derived from oleic
acid (18:1cis-9) and 18:3n 3, and ‘‘soapy’’ odours (octanals) from 18:2n 6 (concentrate fed).
Campo et al. (2003) used a trained sensory panel to
study the flavour of the individual fatty acids 18:1n 9,
18:2n 6 and 18:3n 3, alone or in combination with cysteine and/or ribose. Meaty aromas were much more pronounced when cysteine and ribose were present, i.e.
interactions between Maillard reaction products and fatty
acids. The three fatty acids produced different odour profiles and 18:3n 3 in particular produced high scores for
fishy and linseed/putty. When cysteine and ribose were
present ‘grassy’ was more prevalent.
Other compounds, not derived from fatty acids, may
also contribute to flavour. Skatole (3-methyl indole) is
commonly associated with boar taint in pigs but has been
found in high concentrations in the backfat of beef carcasses that had been fed on grass (Lane & Frazer, 1999).
Interestingly, whilst beef fat from grass-fed animals had
high concentrations of 3-methyl indole, the concentration
in the fat of silage fed animals was more similar to that
of concentrate fed animals (Whittington, Nute, Scollan,
Richardson, & Wood, 2004).
Larick and Turner (1990) attributed flavour differences
between forage-fed and concentrate-fed (feedlot) beef to
both the increased content of PUFA and its lower oxidative stability. It is apparent that antioxidant status of meat
may also have a bearing on flavour and this may contribute
to the difference in acceptability of forage and grain-fed
beef in different studies. In the European Union (EU) many
consumers feel that meat from less intensively-fed animals
has a better taste whilst in the US grass-finished beef is less
acceptable (Mandell, Buchanan-Smith, & Campbell, 1998;
Melton, 1990).
In Belgium, Raes, Balcaen et al. (2003) compared the
fatty acid composition and flavour of Limousin and Belgium Blue retail beef, which was produced locally, with
imported Argentinean and Irish beef. The fatty acid profiles
suggested that the former meat was derived from cereal-fed
animals and the latter were predominantly grass-fed. Sensory analysis and flavour volatile analysis showed that the
grass-fed animals had higher flavour intensity with higher
contents of low molecular weight unsaturated aldehydes
derived from oxidation of long chain PUFA. Finishing
Comparing German Holstein and Simmental bulls on grass
produced meat with a higher n 3 content from the concentrate fed animals, but there was no difference in the
sensory profile except for meat from the grass-finished
beef having a higher ‘bloody’ and ‘fishy’ note (Nuernberg,
Dannenberger et al., 2005).
4.2. Lipid and colour stability
In bovine animals given lipid supplements rich in
PUFA, lipid oxidation can first occur in the plasma lipids,
if the level of antioxidant is limiting, compared to the
amounts of PUFA absorbed from the intestine (Scislowski,
Bauchart, Gruffat, Laplaud, & Durand, 2005). Lipid oxidation produces free radicals and, therefore, may impair the
health of animals (Durand et al., 2005) In muscle tissues
it can promote myoglobin (colour) oxidation and leads to
the formation of rancid odours and flavours. Meat with
more PUFA may be more oxidisable, but when these
PUFA are derived from pasture feeding, they are associated with more antioxidant in the form of a-tocopherol,
N. Scollan et al. / Meat Science 74 (2006) 17–33
and 3.0, respectively, and meat from the animals fed the
maize silage had the worst lipid and colour stability, grass
silage the best and the 50:50 mix being intermediate (O’Sullivan et al., 2002). Animals fed red clover silage, grass
silage, or a 50:50 mix of the two, at 0.7 of intake, had an
increasing content of PUFA in muscle with increasing
red clover silage content but vitamin E concentration
decreased and colour and lipid oxidative stability
decreased. When a fourth group of animals were fed the
red clover silage supplemented with vitamin E, vitamin E
content of muscle, colour and lipid stability was the same
as that in the muscle of 100% grass silage-fed animals
(Fig. 3; Richardson, Costa, Nute, & Scollan, 2005).
When animals are fed a similar basal diet, but fatty acid
composition is altered by the addition of different oils to
the diet, lipid and colour stability can be expected to be
more related to the fatty acid composition than the antioxidant concentration. Steers were fed linseed oil, fish oil or a
Grass
(a)
Colour saturation
Grass /Red clover
28
Red clover
26
Red clover/Vit. E
24
22
20
18
16
14
12
10
1
(b) 6
2
a
3
4
a
b
5
6
7
Days displayed
8
9
10
11
a
5
mg MDA/kg meat
carotenoids and flavonoids (Wood & Enser, 1997), which
stabilise the fatty acids and make the meat more desirable
(Gatellier et al., 2005; Moloney et al., 2001; Richardson
et al., 2004). Charolais cows finished on pasture had higher
vitamin E content in their meat than those finished on
silage and a cereal concentrate and this reduced lipid oxidation (Mercier, Gatellier, & Renerre, 2004). Aberdeen
Angus cross and Holstein–Friesian steers were fed either
perennial ryegrass silage (with 0.15 sugar beet pulp) or concentrates (0.6 barley, 0.2 sugar beet pulp, 0.125 full fat soya
and barley straw) and slaughtered at 14, 19 or 24 months of
age. The vitamin E content of the longissimus muscle was
1.3 and 3.4 mg/kg meat for the concentrate and silage-fed
animals, respectively. When 10 d aged meat was packed
as steaks in a modified atmosphere, this resulted in TBARS
values at 7 d of simulated retail display of 3.8 and 0.6 mg
malonaldehyde equivalents/kg meat, respectively (Richardson et al., 2004). Colour shelf life of the meat from silage
fed animals was extended by 2 d. Hereford cross steers finished on pasture or a sorghum-based feedlot ratio n, each
with or without a 2500 IU/head/day supplementation of
vitamin E had more vitamin E in their meat than those
fed in the feedlot. Supplementation did not increase the
vitamin E content of the grazed animals but brought that
of the feedlot animals up to the level of the grass-fed animals and reduced the rate of fat and colour oxidation
(Yang, Lanari, Brewster, & Tume, 2002). Interestingly,
supplementation of the grass-fed animals with vitamin E
reduced the content of b-carotene in plasma, liver, fat
and muscle (Yang, Brewster, Lanari, & Tume, 2002). When
animals were sampled throughout the year from an Irish
abattoir, those overwintered indoors had better colour stability than those slaughtered from pasture. The vitamin E
content of the muscle was not significantly different
between slaughter periods, but overwintered animals had
more vitamin E in their adipose tissue (Lynch et al.,
2002). As the content of vitamin E in the muscle of many
animals was less than the recommended 3.0–3.5 IU for
optimum stability (Liu, Scheller, Arp, Schaefer, & Williams, 1996) then fatty acid composition may have been
more critical. Meat from pasture finished animals had more
PUFA than overwintered animals and would thus produce
a greater oxidative stress in the meat. O’Sullivan et al.
(2003) studied the effect of six diets varying from 100% forage through combinations of forage and concentrate allowances to a zero-forage with concentrates and straw ration.
The high herbage diet produced the most lipid and colour
stable meat and the high concentrate diet the least with
other diets being intermediate. For production systems in
Uruguay and Argentina, beef finished off grass had higher
vitamin E concentration and better lipid stability than
those finished on concentrates (Descalzo et al., 2000; Realini, Duckett, Brito, Dalla Rizza, & De Mattos, 2004).
The type of forage in a silage-based diet can also affect
lipid and colour stability. Charolais-cross heifers were fed
ad libitum on either maize silage, grass silage or a 50:50
mixture of these. Vitamin E concentration was 2.1, 3.8
4
Grass
Grass/Red clover
Red clover
Red clover/Vit. E
P = 0.001
3
2
1
0
Lipid oxidation
(c)
4
3.5
c
b
a
c
P = 0.001
3
mg/kg meat
28
Grass
Grass/Red clover
Red clover
Red clover/Vit. E
2.5
2
1.5
1
0.5
0
Vitamin E
Fig. 3. Effect of feeding grass silage relative to incremental levels of red
clover silage in the diet on meat quality in steers (a) colour saturation of
loin steaks during retail display in modified atmosphere packs, (b) lipid
oxidation in longissimus after conditioning at 1 C and 10 days display in
over wrapped packs at 4 C, assessed as TBARS, (mg malonaldehyde/kg).
(c) vitamin E content (mg/kg meat); Richardson et al. (2005).
N. Scollan et al. / Meat Science 74 (2006) 17–33
linseed oil/fish oil mix at 30 g oil/kg diet and supplemented
with vitamin E at 345 mg a-tocopherol acetate/kg feed.
The vitamin E concentration in the forequarter meat of
animals receiving the fish oil was reduced 20% but at
5.7 mg/kg muscle was still well above that recommended
for optimum stability, yet longissimus steaks and minced
forequarter muscle were less oxidatively stable than the
other treatments (Vatansever et al., 2000). Feeding a ruminally protected lipid supplement (PLS; see Table 3) rich in
n 6 and n 3 PUFA increased the concentration of total
lipid 18:2n 6 from 120 to 305 mg/100 g and 18:3n 3
from 29 to 139 mg/100 g, vitamin E was reduced 20% to
4.6 mg/kg and colour and lipid oxidative stability were
reduced. This also significantly increased sensorial abnormal flavour and rancidity scores (Scollan, Enser, Richardson, Gulati, Hallett, Wood et al., 2004). Feeding protected
fish oil (rich in DHA) (PFO) at three levels in combination
with free fish oil (rich in EPA and DHA) increased EPA
from 13 to 19 mg/100 g muscle and DHA from 3 to
12 mg/100 g total muscle lipid, did not affect vitamin E
concentration at >5 mg/kg or colour stability, but
increased TBARS at the highest level fed. It also produced
some abnormal flavours but these were insufficient to affect
overall acceptability (Richardson, Hallett et al., 2004). As
the PLS contributed 295 mg extra PUFA and the PFO only
15 mg and whilst the instability of the meat was not as
great for the PFO as PLS, nevertheless the extra double
bonds in EPA and DHA made meat with elevated concentrations of these fatty acids more unstable. If ruminant
meat is to be modified through dietary manipulation it will
be necessary to define a strategy which protects these lipids
from the pro-oxidative environment.
5. Conclusions
It is evident that nutritional value is an important
dimension of beef quality and this is reflected with the
efforts to improve the fatty acid composition of beef.
Increasing the content of n 3 PUFA and CLA and reducing SFA with the net effect of increasing P:S and reducing
n 6:n 3 ratio are important priorities. Nutrition is the
major factor influencing fatty acid composition of beef
whereas both nutrition and genetics affect the level of fat.
Feeding grass and or concentrates-containing linseed or
fish oil results in important beneficial responses in the content of n 3 PUFA, SFA and CLA in beef. Feeding the
forage legume, red clover, results in further enhancements
in PUFA content relative to grass feeding. Studies using
ruminally protected lipids have revealed that muscle does
have a high capacity to deposit n 3 PUFA but strategies
to address the high degree of biohydrogenation of dietary
PUFA in the rumen must be developed.
Knowledge of the relationships between the fatty acid
composition of meat (and other chemical components such
as amino acids and carbohydrates) and sensory attributes
and colour shelf life is increasing. As the content of n 3
PUFA in the meat are increased, sensory attributes such
29
as ‘‘grassy’’, ‘‘greasy’’ and ‘‘fishy’’ score higher and colour
shelf life may be reduced. Novel approaches (antioxidants)
are required to protect n 3 PUFA from oxidation in muscle lipids (especially when higher levels of n 3 PUFA are
achieved >3% n 3 PUFA).
The development of foods with functional properties is a
major growth area and this is likely to continue as consumers demand more foods which offer scope in helping to promote health and prevent disease. In this respect, meat and
meat products (including beef) have an important role to
play. The meat industry has been the slowest section of
the food industry to embrace the functional trend and
incorporate functional ingredients into their products.
However, this is changing as the industry seeks new opportunities to improve sustainability and improve competitiveness with other foods. However, as discussed by Verbeke
(2006) consumers are unlikely to compromise on the taste
of functional foods for health benefits and hence these
foods must seek to deliver health benefits with neutral or
positive impact on taste.
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