Meat Science 84 (2010) 257–270

Contents lists available at ScienceDirect

Meat Science
journal homepage: www.elsevier.com/locate/meatsci

Review

A second look into fibre typing – Relation to meat quality

L. Lefaucheur *
Institut National de la Recherche Agronomique (INRA), Unité Mixte de Recherches 1079, Systèmes d’Elevage, Nutrition Animale et Humaine, Domaine de la Prise,
F-35590 Saint-Gilles, France

a r t i c l e i n f o a b s t r a c t

Article history: Despite intensive research, a large variation in meat quality is still observed in most meat producing spe-
Received 4 March 2009 cies. It is widely accepted that myofibre type composition is an important source of variation in meat
Received in revised form 16 April 2009 quality. However, the identification of specific and universal relationships between myofibre character-
Accepted 3 May 2009
istics, growth performance and meat quality traits remains a challenge. After the presentation of recent
knowledge underlying fibre typing, this review describes the involvements of Ca2+-dependent mecha-
nisms, and the energy state of the myofibres in the control of contractile and metabolic properties, with
Keywords:
a special attention to the AMP-activated protein kinase pathway and mitochondrial compartment. In
Muscle fibres
Myosin heavy chain
order to identify muscle components which could mask specific relationships between fibre type compo-
Energy metabolism sition and meat quality, an analysis of the interactions between myofibres and other muscle cellular com-
Growth ponents is presented. After a brief description of myogenesis, the significance of the total number of
Meat quality fibres, myofibre cross-sectional area and fibre type composition for growth performance and meat quality
is presented. Then, some genetic and environmental factors are proposed as possible tools to control meat
quality trough the modulation of fibre type characteristics. Finally, a conclusion makes the point on bot-
tlenecks still preventing the identification of specific relationships between fibre characteristics, growth
performance and meat quality, and suggests future perspectives such as direct selection on fibre traits
and study of correlated responses, the development of in vitro approaches using cell cultures, manipula-
tion of myogenesis during the fetal period, and the production and use of genetically modified animals.
Ó 2009 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 258
2. Fibre type diversity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 258
2.1. Contractile type . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 258
2.2. Metabolic type. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 259
2.3. Biological characteristics of fibre types . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 260
2.4. Control of contractile and metabolic properties . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 260
2.4.1. Ca2+-dependent pathways . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 260
2.4.2. Energy state . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 260
2.4.3. Mitochondrial respiration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 261
2.5. Relationships between myofibre type composition and other muscle components . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 261
3. Significance of myofibre type for growth performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 261
3.1. Total number of fibres and myofibre cross-sectional area . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 262
3.2. Fibre type composition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 262
4. Fibre type and meat quality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 263
4.1. Total number of fibres and myofibre cross-sectional area . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 263
4.2. Fibre type composition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 264
5. Tools to control meat quality through fibre type composition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 264
5.1. Genetic factors. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 264
5.2. Exercise, ambient temperature and nutrition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 266
6. Conclusion and future perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 266
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 266

* Tel.: +33 2 23 48 56 43; fax: +33 2 23 48 50 80.

E-mail addresses: Louis.Lefaucheur@rennes.inra.fr, louis.lefaucheur@wanadoo.fr

0309-1740/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved.
doi:10.1016/j.meatsci.2009.05.004
258 L. Lefaucheur / Meat Science 84 (2010) 257–270
1. Introduction
In all species raised for meat production, genetic selection and
improvement of nutrition and breeding conditions has led to a
tremendous increase in the efficiency of animal production and
carcass composition by decreasing carcass fatness, and increasing
muscle yield. Several studies suggest that such practice would
have adversely affected some aspects of lean meat quality (Cam-
eron, Nute, Brown, Enser, & Wood, 1999), but the underlying bio-
logical mechanisms remain to be clearly identified. It is widely
accepted that myofibre type composition is an important source
of variation in meat quality (Karlsson, Klont, & Fernandez,
1999). However, because of the highly heterogeneous tissue and
cellular composition of skeletal muscle, and the numerous factors
affecting meat quality (pre-, peri-, and post-mortem), it remains
difficult to identify what muscle biological traits are specifically
involved in determination of meat quality. On average, skeletal
muscle contains about 75% water, 19% protein, 0.5–8% lipid and
1% glycogen, and is composed of several tissues and cell types
including myofibres, along with connective tissue, intramuscular
adipocytes, vascular and nervous tissues. Moreover, myofibres
represent a heterogeneous population differing by structural, con-
tractile, metabolic and physiological properties. The functional
diversity between fibre types, muscles and species has been
achieved during evolution through Darwinian natural selection.
Myofibres can be characterized by their total number (TNF),
cross-sectional area (CSA), length, and contractile and metabolic
properties. Skeletal muscle exhibits remarkable adaptive capabil-
Fig. 1. Serial sections of longissimus muscle from a Large White (A, C, E) and Meishan (B, D, F) pig at 62 kg BW. Histochemical mATPase staining after preincubation at pH 4.35
(A, B). In situ hybridization using 35S labelled MyHC IIx (C, D) and IIb (E, F) riboprobes. The bar indicates 100 lm. Adapted from Lefaucheur et al. (2004).
ities to a number of genetic, nutritional and environmental condi-
tions encountered during the breeding phase of animal
production, such as physical exercise. After a presentation of re-
cent data underlying myofibre typing, the present review will fo-
cus on the significance of myofibre types for growth performance
and meat quality, and will end with some perspectives dealing
with the control of meat quality through manipulation of fibre
type composition during the breeding phase.
2. Fibre type diversity
Myofibres represent 75–90% of the muscle volume and are mul-
tinucleated due to their formation by fusion of myoblasts during
fetal development. Their diameter ranges from 10 to 100 lm and
they are typically classified according to their contractile and met-
abolic properties.
2.1. Contractile type
Based on differences in the sensitivity of the acto-myosin ATP-
ase activity to pH preincubation, three main fibre types have been
conventionally determined by histochemistry in adult skeletal
muscle, i.e. types I, IIA and IIB fibres (Brooke & Kaiser, 1970). The
underlying molecular basis of this typology resides in the polymor-
phism of myosin heavy chains (MyHC), each isoform being en-
coded by a single gene (Weiss et al., 1999). However, four adult
MyHC isoforms have been identified in mouse, rat, guinea pig
and rabbit skeletal muscles, i.e. types I, IIa, IIx and IIb isoforms
 L. Lefaucheur / Meat Science 84 (2010) 257–270 259

(Bär & Pette, 1988; Schiaffino et al., 1989), which lead to revise the
conventional classification to take into account what MyHC were
expressed, i.e. types I, IIa, IIx and/or IIb MyHC. The speed of con-
traction increases in the rank order I < IIa < IIx < IIb (Schiaffino &
Reggiani, 1996). Despite the presence of the IIb MyHC gene in all
mammals, the type IIb MyHC isoform was initially found in small
mammals, and reported to be unexpressed in skeletal muscles of
large mammals such as human, monkey, cattle, horse, goat and
dog (Acevedo & Rivero, 2006; Arguello, LopezFernandez, & Rivero,
2001; Ennion, Sant’Ana Pereira, Sargeant, Young, & Goldspink,
1995; Maccatrozzo, Patruno, Toniolo, Reggiani, & Mascarello,
2004; Maccatrozzo et al., 2007; Rivero, Serrano, Barrey, Valette, &
Jouglin, 1999; Serrano et al., 2001; Smerdu, Karsch-Mizrachi,
Campione, Leinwand, & Schiaffino, 1994; Smerdu, Strbenc, Mezna-
ric-Petrusa, & Fazarinc, 2005; Tanabe, Muroya, & Chikuni, 1998;
Toniolo et al., 2005, 2007). Until recently, the hypothesis among
researchers was that type IIb MyHC, the fastest isoform, was only
expressed in small mammals in relation to the relative higher
speed of contraction of their muscles compared to large species.
However, recent data using immunocytochemistry, in situ hybrid-
ization, and real time RT-PCR demonstrated that the IIb MyHC iso-
form was highly expressed in glycolytic muscles of the pig and
llama (Da Costa, Blackley, Alzuherri, & Chang, 2002; Graziotti,
Palencia, Delhon, & Rivero, 2004; Graziotti, Rios, & Rivero, 2001;
Lefaucheur et al., 1998; Lefaucheur, Ecolan, Plantard, & Gueguen,
2002; Lefaucheur, Milan, Ecolan, & Le Callennec, 2004). Therefore,
the expression of the IIb MyHC was not restricted to small mam-
mals as previously suggested, and the conventional histochemical
fibre typing in types I, IIA and IIB (Brooke & Kaiser, 1970) appeared
to be not well adapted for pig and llama skeletal muscles where
four MyHC are present. The limitation of the conventional fibre
Thus, a large amount of ATP is hydrolyzed during contraction
through activation of the acto-myosin ATPase, and a harmonious
functioning needs a balance between ATP consumption and pro-
duction to prevent ATP depletion. Two major metabolic pathways
are used to regenerate ATP in skeletal muscle, i.e. the aerobic or
oxidative pathway through which glycogen, glucose, amino acids,
ketone bodies, and lipids can be oxidized in the mitochondria with
a high oxygen requirement, and the anaerobic or glycolytic path-
way through which intrafibre glycogen stores are rapidly con-
verted to lactate with no oxygen requirement. Aerobic
metabolism is sufficient to cover energy demand when oxygen is
adequate and muscle is working with low intensity, but if contrac-
tion proceeds faster and with high intensity, oxygen becomes lim-
iting and the muscle will have to use the rapid anearobic glycolytic
pathway to supply energy. The relative importance of these two
metabolic pathways has been used to type myofibres as oxidative,
oxido-glycolytic or glycolytic (Ashmore & Doerr, 1971; Peter, Bar-
nard, Edgerton, Gillespie, & Stemple, 1972). A mitochondrial en-
zyme, succino-dehydrogenase (SDH), is commonly used to type
myofibres as red (R, SDH+) or white (W, SDH) by histochemistry.
By combining conventional acto-myosin ATPase after preincuba-
tion at pH 4.35 with SDH staining on serial sections, pig longissi-
100 100
80 80
60 60
%

%
typing in the pig is clearly illustrated when comparing longissimus
40 40
muscle fibre type composition between the Large White (LW) and
Meishan breeds (Fig. 1). Indeed, no difference in the proportion of
conventional types I, IIA and IIB fibres was observed between the 20 20
two breeds, even though MyHC IIb and IIx were the prominent iso-
forms in LW and Meishan pigs, respectively (Lefaucheur et al.,
0 0
2004). Recently, expression of the IIb MyHC isoform has been re- s sa a ax x xb b
IIA

W
I

IIB

IIB

ported in longissimus and semitendinosus muscles of few bulls

within the Blonde d’Aquitaine breed (Picard & Cassar-Malek, 2009). Fig. 2. Correspondance between the conventional histochemical fibre type classi-
Myosin heavy chain is the most abundant protein expressed in fication (I, IIA, IIBR and IIBW, left) and the presence of the myosin heavy chains I (s),
skeletal muscle, comprising about 35% of the protein pool. The IIa (a), IIx (x) and IIb (b) revealed by immunocytochemistry (right) in Large White
ATPase activity of MyHC is fundamental in determining the rate pig longissimus muscle at 108 kg BW. Hybrid fibres are noted sa, ax and xb. Black
and white areas denote succino-dehydrogenase positive (oxidative) and negative
of cross-bridge cycling, and thus the speed of contraction. At least
(glycolytic) fibres, respectively. Percentages have been estimated from a total of
eight distinct skeletal MyHC genes are present in mammalian stri- 13.000 myofibres using computerized image analysis. Lefaucheur et al.
ated muscles, including two developmental (embryonic and fetal), (unpublished).
one slow (type I or b-cardiac), one a-cardiac, three adult fast type II
MyHC (IIa, IIx, and IIb), and the extraocular MyHC, a specialized
isoform. These genes are located in two clusters in all mammals Table 1
Biological characteristics of individual fibre typesa. Adapted from Bacou and Vigneron
studied so far (Davoli et al., 2002; Mahdavi, Chambers, & Nadal-
(1988), Essén-Gustavsson et al. (1994), Pette and Staron (2000), Quiroz-Rothe and
Ginard, 1984; Shrager et al., 2000; Weiss et al., 1999; Weiss, Rivero (2004), Schiaffino and Reggiani (1996).
Schiaffino, & Leinwand, 1999). The skeletal MyHC gene cluster con-
I IIa IIx IIb
tains the embryonic, IIa, IIx, IIb, fetal and extraocular MyHC in this
order, whereas the cardiac cluster consists in the b MyHC (slow Contraction speed + +++ ++++ +++++
type I) upstream of the a-cardiac MyHC gene. Expression of MyHC Myofibrillar ATPase + +++ ++++ +++++
Oxidative metabolism +++++ ++++, +++++ +, ++ +
is reported to be transcriptionally regulated (Cox & Buckingham,
Glycolytic metabolism + ++++ ++++ +++++
1992). However, very recent data suggest that MyHC gene regula- Hexokinase +++++ +++ + +
tion would be more complex than previously appreciated due to GLUT-4 +++++ +++ + +
the presence of bidirectional intergenic promoters coordinating Phosphocreatine + +++++ +++++ +++++
Glycogen + +++++ ++++ +++++
the expression of the different MyHC (Haddad et al., 2008; Rinaldi
Triglycérides +++++ ++ + +
et al., 2008). Vascularization +++++ +++ +, ++ +
Myoglobine +++++ ++++ ++ +
2.2. Metabolic type Buffering capacity + ++++ +++++ +++++
Diameter ++ +, ++ ++++ +++++
Fatigue resistance +++++ ++++ ++ +
Skeletal muscle is characterized by a dramatic increase in en-
a
ergy consumption and turnover in response to physical exercise. +, very low; ++, low; +++, medium; ++++, high; +++++, very high.
260 L. Lefaucheur / Meat Science 84 (2010) 257–270
mus muscle has been shown to contain 9.5% type I, 6.5% type IIA,
10% type IIBR (SDH+), and 74% type IIBW (SDH) (Larzul et al.,
1997). The correspondence between this classification and the
presence of the MyHC I (s), IIa (a), IIx (x) and IIb (b) revealed by
immunocytochemistry shows that fibres containing either IIx,
(IIx + IIb) (hybrid fibres), or only IIb MyHC are mostly IIBW fibres
(Fig. 2), denoting that conventional histochemical fibre typing in
types I, IIA, IIBR and IIBW cannot fully distinguish fibres containing
different MyHC, in particular IIx and IIb MyHC.
2.3. Biological characteristics of fibre types
Individual fibre types exhibit different contractile, metabolic,
physiological, chemical and morphological characteristics as pre-
sented in Table 1. Slow-twitch oxidative type I fibres exhibit low
myofibrillar and sarcoplasmic reticulum (SR) ATPase activities,
and can sustain prolonged low power work in association with a
well-developed oxidative metabolism, an efficient vascularization,
and a small diameter. These fibres exhibit a low excitation thresh-
old (high Ca2+ sensitivity) and use a large amount of energy in vivo
because they are often recruited to sustain low intensity contrac-
tions for basic movements. They are poor in glycogen, rich in myo-
globine and triglycerides, and highly resistant to fatigue. It is well
established that glucose uptake (Bonen, Tan, & Watson-Wright,
1981), GLUT-4 levels and hexokinase activity (Kern et al., 1990),
incorporation of 14C-glucose into glycogen (Bär & Blanchaer,
1965), turnover of glycogen (Villa-Moruzzi, Locci-Cubeddu, &
Bergamini, 1979), number of insulin receptors (Lefaucheur, Le
Peuch, Barenton, & Vigneron, 1986), and insulin sensitivity (Henriksen
et al., 1990) are higher in slow-twitch type I than fast-twitch type II
fibres, in particular type IIb glycolytic fibres. On the opposite, gly-
colytic types IIb fibres exhibit high myofibrillar and SR ATPase
activities, and can sustain brief and intense contractions fueled
by immediate availability of phosphocreatine and degradation of
local glycogen through the glycolytic pathway. These fibres exhibit
a high excitation threshold and do not use a large amount of en-
ergy in vivo because they are only occasionally recruited to sustain
violent movements of short duration, e.g. to escape immediate
danger. In association with a low vascularization and a large diam-
eter, glycolytic types IIb fibres are rich in glycogen, poor in myoglo-
bine and triglycerides, and highly fatigable. Their low GLUT-4
levels and hexokinase activity denote a predominant utilization
of locally stored glycogen during intense contraction, with produc-
tion of lactate. Characteristics of type IIx fibres are close to those of
IIb fibres, excepted that they speed of contraction is lower and
their oxidative metabolism slightly higher. Type IIa fibres exhibit
intermediate contractile and metabolic properties between types
I and IIx fibres.
Intramyofibre lipids (IMFL), i.e. those contained within myofi-
bres, can be subdivided into phospholipids, triacylglycerols
(TAG), mono- and diacylglycerols, cholesterol, cholesteryl esters,
and free fatty acids. The level of TAG (oil red O staining) is high
in slow-twitch type I fibres, moderate in oxido-glycolytic IIA fibres,
and very low in glycolytic IIB fibres (Essén-Gustavsson, Karlsson,
Lundstrom, & Enfält, 1994; Malenfant et al., 2001). Phospholipids
are the main constituents of cellular membranes, and their contri-
bution to total intramuscular fat (IMF) varies between 0.7% and
0.9%, and is about 30% higher in oxidative than glycolytic muscles,
likely in relation to the higher mitochondrial content of oxidative
muscles (Alasnier, Rémignon, & Gandemer, 1996; Leseigneur-Mey-
nier & Gandemer, 1991). Positive correlations between muscle
insulin resistance and accumulation of intramyofibre TAG have
been reported (van Loon & Goodpaster, 2006). However, this corre-
lation does not seem to represent a functional relationship because
(1) type I fibres contain more TAG and are more sensitive to insu-
lin, and (2) endurance training increases both intramyofibre TAG
content and insulin sensitivity. Therefore, the level of intramyofi-
bre TAG does not seem to be a causal factor inducing insulin resis-
tance which would rather be mediated by intermediate lipid
metabolites, such as diacylglycerol and/or ceramide (Turinsky,
O’Sullivan, & Bayly, 1990).
2.4. Control of contractile and metabolic properties
2.4.1. Ca2+-dependent pathways
In normal cells, basal sarcoplasmic Ca2+ level is maintained
close to 107 M, which is about 104-fold lower than in SR. During
contraction, membrane depolarization stimulates the release of
Ca2+ from the SR, which increases sarcoplasmic Ca2+ concentration
up to 100-fold. The increase in sarcoplasmic Ca2+, in turn, serves as
a second messenger through interaction with troponin C to trigger
contraction, and with calcineurin, a Ca2+/calmodulin-activated ser-
ine-threonine phosphatase, Ca2+-calmodulin-dependent protein
kinases (CaMK), and Ca2+-dependent protein kinase C (Jorgensen,
Jensen, & Richter, 2007; Koulmann & Bigard, 2006; Reznick & Shul-
man, 2006) to modulate numerous regulatory pathways. Calcium
ions can also modulate glycogen phosphorylase activity (Tate,
Hyek, & Taffet, 1991). Thus, Ca2+ is a highly versatile intracellular
signal that operates over a wide spatiotemporal range to regulate
many different cellular processes in skeletal muscle. Low and sus-
tained repetitive global Ca2+ transients in slow-twitch fibres and
high and rapid localized spikes of Ca2+ in fast-twitch fibres are cen-
tral for a selective control of gene expression and metabolic path-
ways in different fibre types. For example, only Ca2+ transients
corresponding to those encountered in slow fibres can activate cal-
cineurin to stimulate the activation of many slow-fibre genes in-
volved in contractile process, Ca2+ uptake and energy metabolism
(Naya et al., 2000). In addition to SR, mitochondria have also been
shown to actively participate in the regulation of Ca2+ homeostasis
by rapidly and efficiently accumulating Ca2+ in the mitochondrial
matrix (Brini et al., 1997). Altogether, Ca2+ ions are heteroge-
neously distributed within skeletal muscle, and Ca2+ flux and/or
leak is a fundamental process influencing both in vivo muscle biol-
ogy, as well as post-mortem (p.m.) conversion of muscle to meat.
2.4.2. Energy state
Because increases in free ADP and AMP levels during contrac-
tion are higher in fast-twitch glycolytic than slow-twitch oxidative
fibres, free ADP and AMP levels are particularly important signals
for the metabolic control of ATP resynthesis through the anaerobic
pathway in glycolytic fibres (Hochachka & McClelland, 1997). In-
deed, AMP has been shown to be an allosteric activator of glycogen
phosphorylase and phosphofructo kinase (Longnus, Wambolt, Par-
sons, Brownsey, & Allard, 2003; Miyamoto et al., 2007). In addition,
AMP stimulates the activity of AMP-activated protein kinase
(AMPK), a fuel gauge monitoring the status of cellular energy
(Hardie & Hawley, 2001). AMP binding to the c-subunit of AMPK,
which binding is antagonized by high ATP concentrations, stimulates
AMPK activity both directly by an allosteric mechanism, and indi-
rectly through phosphorylation of AMPK on threonine 172 of the a
subunit (Hardie & Sakamoto, 2006; Hawley et al., 1995). Activation
of AMPK switches on pathways that generate ATP, such as glycol-
ysis, glucose and fatty acid uptake, fatty acid oxidation, and mito-
chondrial biogenesis, whereas it switches off ATP-consuming
processes such as glycogen, fatty acid and protein synthesis (Har-
die & Hawley, 2001; Jorgensen et al., 2004; Kahn, Alquier, Carling,
& Hardie, 2005; Kurth-Kraczek, Hirshman, Goodyear, & Winder,
1999; Long & Zierath, 2005; Marsin et al., 2000; Wojtaszewski, Jor-
gensen, Hellsten, Hardie, & Richter, 2002). However, the promoting
effect of AMPK on glucose uptake can induce an accumulation of G-
6-P, a potent allosteric activator of glycogen synthase (GS), which
seems to override the inhibition of glycogen synthesis induced
 L. Lefaucheur / Meat Science 84 (2010) 257–270
by phosphorylation of GS by AMPK, thus leading to an accumula-
tion of muscle glycogen. AMPK is a heterotrimeric serine/threonine
protein kinase composed of a catalytic a-subunit (a1 or a2), and
regulatory b- (b1 or b2) and c- (c1, c2, and c3) subunits. Expres-
sion of a1, b1, c1 and c2 is ubiquitous, a2 and b2 are mostly ex-
pressed in skeletal and cardiac muscles and liver, whereas c3 is
exclusively expressed in skeletal muscle. Interestingly, c3 is more
highly expressed in fast-twitch glycolytic than oxido-glycolytic fi-
bres as a2b2c3 heterotrimers, whereas it is virtually undetectable
in slow-twitch oxidative fibres (Barnes et al., 2004; Mahlapuu
et al., 2004; Yu, Fujii, Hirshman, Pomerleau, & Goodyear, 2004).
In addition, 5-aminoimidazole-4-carboxamide-1-b-D-ribonucleo-
side (AICAR), a specific AMPK activator, has been shown to have
no effect on AMPK activity, GLUT-4 expression and glucose uptake
in the slow-twitch rat soleus muscle (Ai et al., 2002; Balon & Jas-
man, 2001; Buhl et al., 2001; Wright, Geiger, Holloszy, & Ho-Han,
2005).
In addition to LKB1, Ca2+/calmodulin-dependent kinase kinase
(CaMKK) would also be an upstream kinase of AMPK (Hawley
et al., 2005; Hurley et al., 2005; Woods et al., 2005), suggesting po-
sitive interrelations between Ca2+ and AMPK pathways. However, a
chronic exposure to elevated cytosolic Ca2+ concentration has re-
cently been shown to block AMPK-induced GLUT-4 expression in
muscle (Park et al., 2009), denoting complex interconnections be-
tween Ca2+ and AMPK pathways.
2.4.3. Mitochondrial respiration
The numerous mitochondria encountered in oxidative fibres ex-
hibit a radial gradient distribution with a higher density in the sub-
sarcolemmal area, whereas the much less abundant mitochondria
of glycolytic fibres are homogeneously distributed throughout the
fibre (Swatland, 1984). Beyond these differences in the amount and
distribution of mitochondria between fibre types, the regulation of
mitochondrial respiration has been shown to differ between fibre
types. First, respiration is more sensitive to the inhibitory effect
of physiological concentrations of ATP in mitochondria isolated
from fast- than slow-twitch muscle (Gueguen, Lefaucheur, Ecolan,
Fillault, & Herpin, 2005). Second, data obtained on permeabilized
fibres demonstrate that stimulation of mitochondrial respiration
by ADP is more sensitive in types IIb and IIx (Km = 8 lM) than IIa
(72 lM) and I (212 lM) fibres, suggesting that mitochondrial res-
piration is strongly regulated by free ADP in types IIb and IIx fibres,
once ATP level tends to decrease (Gueguen, Lefaucheur, Fillault, &
Herpin, 2005; Gueguen, Lefaucheur, Fillaut, Vincent, & Herpin,
2005). In contrast, the addition of creatine or AMP strongly stimu-
lates mitochondrial respiration in type I fibres, and has no effect in
types IIb and IIx fibres, denoting a strong coupling between mito-
chondrial creatine (CK) and adenylate (AK) kinases and oxidative
phosphorylation in type I fibres, and a weak coupling in glycolytic
fibres, IIA fibres are intermediate. Thus, the high levels of phospho-
creatine and cytosolic MM-CK in glycolytic fibres function as an
energy buffer coupled with rapid glycolytic ATP production during
contraction, and mitochondrial ATP regeneration during recovery.
On the opposite, the mitochondrial CK, in association with the
cytosolic muscle CK (MM-CK) functions as a channelling system
to efficiently transfer ATP and ADP between mitochondria and sites
of ATP consumption via successive phosphocreatine and creatine
cyclings in type I fibres.
2.5. Relationships between myofibre type composition and other
muscle components
Intramuscular fat (IMF) content is generally reported to be pos-
itively related with meat tenderness, juiciness and flavor (Fernan-
dez, Monin, Talmant, Mourot, & Lebret, 1999), even though these
261
relationships were not always detected (Blanchard, Willis, Warkup,
& Ellis, 2000; Rincker, Killefer, Ellis, Brewer, & Mckeith, 2008; Rinc-
ker, Killefer, Matzat, Carr, & Mckeith, 2009). In pork shops, increas-
ing IMF content up to 2.5–3% is suggested to improve flavor,
juiciness and tenderness (Devol et al., 1988), whereas a higher
IMF content has adverse effects on consumer acceptability due to
increased visibility of fat in meat (marbling). Total IMF is com-
posed of triglycerides and phospholipids which represent 0.5–7%
and about 0.5% of fresh pig longissimus muscle, respectively
(Faucitano, Rivest, Daigle, Levesque, & Gariepy, 2004; Leseigneur-
Meynier & Gandemer, 1991). A small amount of triglycerides is
localized as droplets mostly within type I myofibres, whereas an
overwhelming amount of triglycerides is located in intramuscular
adipocytes mostly grouped along the perimysium, or interspersed
between myofibres (Essén-Gustavsson et al., 1994; Gondret, Mou-
rot, & Bonneau, 1998). It is often stated that red oxidative muscles
contain more total IMF than white glycolytic muscles. However, a
careful analysis of available data does not confirm this statement,
and shows that the amount and size of intramuscular adipocytes
within a muscle would not be related to its fibre type composition.
This has been shown many times in pig within populations (Eggert,
Depreux, Schinckel, Grant, & Gerrard, 2002; Fiedler, Nurnberg,
Hardge, Nurnberg, & Ender, 2003; Larzul et al., 1997), between
genotypes (Essén-Gustavsson & Fjelkner-Modig, 1985; Lebret
et al., 1999) and different muscles (Beecher, Cassens, Hoekstra, &
Briskey, 1965; Leseigneur-Meynier & Gandemer, 1991), and in
feeding experiments (Candek-Potokar, Lefaucheur, Zlender, &
Bonneau, 1999; Essén-Gustavsson et al., 1994). Data from our lab-
oratory even show that IMF content can be up to three times higher
in the white glycolytic than red oxidative portion of pig semitendi-
nosus muscle, which is consistent with other data reporting that
the frequency of IIBW fibres and IMF content can be positively cor-
related (Henckel, Oksbjerg, Erlandsen, Barton-Gade, & Bejerholm,
1997). Finally, it is noteworthy that most intramuscular adipocytes
are located in the perimysium, in the vicinity of glycolytic fibres
which are the prominent fibre type at the periphery of the myofi-
bre fascicles. All these data denote no universal relationship be-
tween intramuscular adipocyte content and fibre type
composition, and suggest that both characteristics are rather inde-
pendent and can be manipulated separately. On the opposite, a
strong positive genetic correlation (rg = 0.68) between IMF content
and myofibre CSA has been observed in Large White pigs (Larzul
et al., 1997). In most cases, phenotypic and genetic correlations be-
tween animal general fatness and total IMF content are positive,
even though the genetic correlation only reached 0.30 in pig
(Sellier, 1998), showing that IMF is not totally genetically related
to body fatness (Suzuki et al., 2005).
Collagen, one of the main components of muscular connective
tissue, plays an important role in binding myofibres together and
into fascicules. In the rat, slow-twitch muscles contain more colla-
gen than fast-twitch muscles (Kovanen, Suominen, & Heikkinen,
1984). However, no clear relationship between collagen content
and fibre type composition has been reported in livestock species.
As the animals get older, covalent crosslinks form, linking individ-
ual collagen molecules together and making connective tissue
more rigid and less soluble. The increase in collagen concentration
and the decrease in its solubility are well known to decrease ten-
derness of meat, but no specific relationship with muscle fibre type
composition has been documented.
3. Significance of myofibre type for growth performance
In most farm mammals and birds, myogenesis is at least a bi-
phasic phenomenon involving the successive differentiation of a
primary and secondary generation of myotubes during the fetal
262 L. Lefaucheur / Meat Science 84 (2010) 257–270
TNF CSA, µm 2
W cle, larger myofibres and a decreased carcass lean meat content at
110 kg BW
8000
R
100
90 Age, d 165 d
Age, d
Birth Birth
(114 d)
Fig. 3. Schematic representation of changes in the total number of fibres (TNF) and
their cross-sectional area (CSA) in future white (W) and red (R) myofibres during
development in the pig.
period. The number of secondaries around each primary varies
from between 5 and 9 in mouse and rat (Ontell, Bourke, & Hughes,
1988; Ross, Duxson, & Harris, 1987) to over 20 in larger species,
such as pig (Stickland & Handel, 1986). The total number of fibres
(TNF) is generally considered to be established by 90 dg in the pig,
i.e. after 80% of gestation (Wigmore & Stickland, 1983), and by
180 dg in cattle, i.e. after 66% of gestation (Picard, Lefaucheur, Ber-
ri, & Duclos, 2002), denoting a higher maturity in cattle. A third
generation of fibres forming around some secondaries has been de-
scribed shortly after birth in large species such as sheep, pig, hu-
man and cattle (Ashton, Bayol, Mcentee, Maltby, & Stickland,
2005; Lefaucheur, Edom, Ecolan, & Butler-Browne, 1995; Masca-
rello, Stecchini, Rowlerson, & Ballocchi, 1992). Contrary to TNF,
myofibre CSA remains rather constant during gestation, and dra-
matically increases postnatally, to a greater extent in future glyco-
lytic than oxidative fibres (Fig. 3). Contractile and metabolic
maturations of myofibres mostly occur either at the end of gesta-
tion in cattle (Gagniere, Picard, Jurie, & Geay, 1999), or during
the first post-natal weeks in less mature species such as pig
(Lefaucheur & Vigneron, 1986) and rabbit (Gondret, Lefaucheur,
Dalbis, & Bonneau, 1996).
3.1. Total number of fibres and myofibre cross-sectional area
Muscle mass is related to TNF, myofibre CSA and length of
myofibres. Between species variability of TNF is much higher than
that of fibre CSA (Plaghki, 1985; Rehfeldt, Fiedler, & Stickland,
2004). At a constant body weight, a negative phenotypic correla-
tion, between 0.3 to 0.8 in pig, is reported between TNF and
CSA (Kim et al., 2008; Rehfeldt, Fiedler, Dietl, & Ender, 2000),
and a positive correlation between TNF and lean tissue growth
potential is usually reported (Dwyer, Fletcher, & Stickland, 1993;
Handel & Stickland, 1988; Henckel et al., 1997; Kim et al., 2008;
Luff & Goldspink, 1967). The last correlation is very obvious when
comparing double-muscled with normal cattle (Holmes & Ash-
more, 1972). Larzul et al. (1997) found a positive genetic correla-
tion between lean tissue growth rate and myofibre mean CSA
(rg = 0.47); however, a careful examination of the literature shows
a controversial relationship between carcass lean meat content
and fibre CSA. This controversy can be explained by the fact that
carcass lean content and muscle growth potential would be pri-
marily dependent on TNF. Therefore, one should first take into ac-
count TNF before studying any relationships between muscle
development and myofibre CSA. Indeed, a strong positive correla-
tion between myofibre CSA and muscle development is expected
at a constant TNF. Sometimes, a negative correlation is reported
between lean meat content and myofibre CSA, likely due to differ-
ences in TNF. This is the case in low birth weight piglets which
have been shown to exhibit a lower TNF in semitendinosus mus-
commercial slaughter weight than normal birth weight piglets, as
well as increased adiposity and IMF content (Gondret, Lefaucheur,
Juin, Louveau, & Lebret, 2006; Hegarty & Allen, 1978; Miller, Gar-
wood, & Judge, 1975; Powell & Aberle, 1981; Rehfeldt & Kuhn,
2006). These differences at equal slaughter weight are likely re-
lated to a higher physiological maturity of low birth weight pig-
lets where the plateau of muscle fibre hypertrophy is achieved
earlier because of a lower TNF. Overall, a high TNF combined with
moderate mean myofibre CSA is a way to increase muscle growth
potential without decreasing the oxidative capacity which could
be induced by excessive myofibre hypertrophy. Growth in myofi-
bre length is also likely an important mechanism to explain mus-
cle growth and the increase in CSA of some muscles such as that
of longissimus where myofibres make a 25° angle to the vertebral
axis (Davies, 1972). However, growth in length of myofibres has
been poorly studied.
3.2. Fibre type composition
Comparisons between wild and domesticated animals within
different species suggest that selection for increased growth rate
and lean meat content has increased myofibre CSA, and shifted
muscle metabolism towards a more white glycolytic and less red
oxidative type (Ashmore, 1974; Rahelic & Puac, 1981; Ruusunen
& Puolanne, 2004; Solomon & West, 1985; Weiler, Appell, Kremser,
Hofäcker, & Claus, 1995). A comparison between adult LW
(28.2 months, 260 kg) and Meishan pigs (25.6 months, 184 kg)
supports this hypothesis in domesticated pigs in that LW pigs were
leaner and exhibited higher TNF, larger IIB glycolytic fibres, and
were more glycolytic and less oxidative than Meishan (Bonneau,
Mourot, Noblet, Lefaucheur, & Bidanel, 1990). Other comparisons
between different pig breeds suggests that high muscularity is pos-
itively related with a high abundance of MyHC IIb transcript (Wim-
mers et al., 2008). Within the LW breed, two selection experiments
found a positive relationship between the percentage of slow-
twitch type I fibres in longissimus muscle and carcass fatness
(Brocks, Hulsegge, & Merkus, 1998; Lefaucheur et al., 2000). A sim-
ilar trend was observed between the percentage of oxidative fibres
and carcass fatness in the sheep (Kadim, Purchas, Davies, Rae, &
Barton, 1993). However, these results have not been confirmed in
other experiments carried out in conventional European domesti-
cated pigs (Henckel et al., 1997; Karlsson et al., 1993; Larzul
et al., 1997; Oksbjerg et al., 2000; Ruusunen, Sevonaimonen, &
Puolanne, 1996; Seideman, Crouse, & Mersmann, 1989; Tribout
et al., 2004). In particular, an increase in carcass lean percentage
and lean tissue growth rate were both positively related to both
glycolytic and oxidative metabolisms in longissimus (Henckel
et al., 1997; Karlsson et al., 1993). On the opposite, two experi-
ments implemented to estimate the realized genetic trends in
French LW pigs from 1977 to 1998 (Tribout et al., 2004), and
Danish Landrace pigs from 1976 to 1995 (Oksbjerg et al., 2000)
confirmed the expected dramatic improvement in growth rate
and carcass leanness, but surprisingly found a decreased activity
of lactate dehydrogenase, a glycolytic enzyme, in longissimus mus-
cle. Finally, other studies did not find any significant correlations
between lean tissue growth rate, or loin eye area, and fibre type
composition in pig longissimus muscle (Candek-Potokar et al.,
1999; Larzul et al., 1997; Ryu, Rhee, & Kim, 2004). Taken together,
strong relationships between fibre type composition and growth
performance can be found when comparing extreme genetic mod-
els, such as wild versus domesticated animals, but many of these
relationships become controversial when studied within conven-
tional domesticated animals.
 L. Lefaucheur / Meat Science 84 (2010) 257–270
4. Fibre type and meat quality
Following exsanguination, skeletal muscles become isolated
structures and are no more supplied in oxygen and exogenous
nutrients. ATP production is necessary to keep the muscle in the
relaxed state, and the formation of permanent acto-myosin cross-
bridges occur when ATP level decreases, leading to rigor mortis. It
is well documented that p.m. conversion of muscle to meat is ini-
tiated by Ca2+ leaking within the muscle and subsequent activation
of ATPases, modification of adenine nucleotide concentrations, and
degradation of glycogen to lactic acid through glycolysis. This leads
to acidification of the meat with variable rate and extent of pH de-
crease depending on the rate of H+ production and muscle buffer-
ing capacity. In addition to these physicochemical changes,
proteolytic systems are stimulated, leading to p.m. maturation of
the meat. Meat quality is known to be influenced by numerous fac-
tors such as genetic, pre-slaughter and slaughter conditions, p.m.
processing, as well as nutritional and environmental conditions
during the rearing phase. It is commonly reported that muscle fibre
composition influences many aspects of meat quality, including
colour, water holding capacity, tenderness, juiciness and flavor.
However, identifying the specific relationships between meat qual-
ity and myofibre characteristics, i.e. TNF, myofibre CSA and fibre
types, remains a difficult task as discussed in the following
subsections.
4.1. Total number of fibres and myofibre cross-sectional area
As previously reported, TNF and myofibre CSA are frequently
negatively correlated at a given body weight. In pig, it is widely re-
ported that increasing myofibre CSA would be detrimental for
meat quality, in particular water holding capacity and tenderness
(Rehfeldt et al., 2000). Several studies found hypertrophy of fast-
twitch oxido-glycolytic fibres to be more specifically detrimental
to meat tenderness and water holding capacity (Larzul et al., 1997;
Lengerken, Maak, Wicke, Fiedler, & Ender, 1994; Maltin et al.,
1997). Several major genes (Table 2), such as mutated Ryr1, IGF-
II or RN (‘‘Rendement Napole”) genes in pigs (Essén-Gustavsson,
Karlstrom, & Lundstrom, 1992; Lebret et al., 1999; Milan et al.,
2000; Van den Maagdenberg, Stinckens, Lefaucheur, Buys, & de
Smet, 2008), the double-muscling gene in cattle (Grobet et al.,
1997), the Callipyge gene in sheep (Carpenter, Rice, Cockett, &
Snowder, 1996; Vuocolo et al., 2007), or treatments with b-ago-
nists (Dunshea, D’Souza, Pethick, Harper, & Warner, 2005), growth
hormone (Bonneau, 1991), and steroids (Clancy, Lester, & Roche,
1986; Fritsche, Solomon, Paroczay, & Rumsey, 2000) all induce an
Table 2
Effects of some major genes on total number of fibres (TNF), myofibre cross-sectional
area (CSA) and percentage glycolytic fibres (% W) of valuable muscles in different
species. =, no effect; nd, not determined.
Pig Cattle Sheep
Ryr1 a
RN b
IGF-II c
Myostatin d
Callipygee
TNF =, = = =
CSA
Red fibres nd = =
White fibres = nd
%W = data in pigs suggest that increasing only TNF would not be suffi-
a
Lindholm, Persson, Jonsson, and Andrén (1977), Essén-Gustavsson et al. (1992),
Pedersen et al. (2001), Depreux, Grant, and Gerrard (2002).
b
Lebret et al. (1999).
c
Van den Maagdenberg et al. (2008).
d
Holmes and Ashmore (1972), Ashmore, Parker, Strokes, and Doerr (1974),
Swatland and Kieffer (1974), West (1974).
e
Koohmaraie, Shackelford, Wheeler, Lonergan, and Doumit (1995), Carpenter
et al. (1996).
263
increase in myofibre CSA, sometimes in a fibre type dependant
manner, and influence to variable degrees some meat quality traits,
such as water holding capacity, colour and sensory quality (Cannon
et al., 1995). However, this kind of correlations is not sufficient to
conclude that large myofibre CSA is the causal factor of meat qual-
ity deterioration. Indeed, the mechanism leading to meat quality
deterioration in the mutated Ryr1 pigs is a punctual mutation in
the SR Ca2+ channel, leading to an abnormally high release of
Ca2+ in the sarcoplasm and rapid early p.m. drop in pH, giving rise
to Pale Soft and Exudative meat (PSE). In RN carrier pigs, the R225Q
RN single point mutation in the c3-subunit of AMPK increases
AMPK activity (Park et al., 2009), in accordance with data from
similar AMPK mutant mice where the mutation has been shown
to eliminate the allosteric regulation of AMPK by ATP/AMP, result-
ing in increased basal AMPK activity and muscle glycogen storage
(Barnes et al., 2004). This dominant RN mutation is responsible for
a 70% selective increase of glycogen content in glycolytic muscles,
whereas oxidative muscles are unaffected (Estrade, Vignon, Rock, &
Monin, 1993; Lebret et al., 1999; Marinova, Lefaucheur, Fernandez,
& Monin, 1992; Monin, Mejenes-Quijano, Talmant, & Sellier, 1987),
leading to a low ultimate pH and acid meat with low water holding
capacity in glycolytic muscles (Leroy et al., 2000). Mutations and/or
deletions in the bovine myostatin gene is the causal factor explain-
ing the double-muscled phenotype mostly due to a dramatic in-
crease in TNF and, to a lower extend, a specific hypertrophy of
glycolytic fibres (Holmes & Ashmore, 1972; Ouhayoun & Beau-
mont, 1968). The superior tenderness of double-muscled cattle
has been attributed to a lower total and higher soluble collagen
content (Ngapo et al., 2002). In Callipyge sheep, a causative point
mutation is located in an intergenic region and the mechanism
leading to the specific increased CSA of fast myofibre could rather
be a reduced protein degradation, inducing a lower p.m. proteoly-
sis, maturation and tenderization of meat (Lorenzen et al., 2000). In
b-agonist treated animals, in particular lambs, the decreased meat
tenderness was specifically due to a reduced p.m. maturation be-
cause of an increased calpastatin activity and decreased proteolysis
(Koohmaraie, Shackelford, Muggli-Cockett, & Stone, 1991).
Other studies do not support a negative influence of myofibre
CSA on meat quality. Thus, a strong positive genetic correlation
(rg = 0.68) was found in longissimus muscle of Large White pigs be-
tween myofibre CSA and IMF content (Larzul et al., 1997), a char-
acteristic generally associated with improved tenderness and
flavor of pork. In cattle, the relationship between tenderness and
mean fibre CSA is highly controversial (Renand, Picard, Touraille,
Berge, & Lepetit, 2001; Seideman & Crouse, 1986). Surprisingly, a
study carried out in broiler breast muscle recently showed a posi-
tive influence of myofibre CSA on meat quality through a decreased
muscle glycogen content, higher ultimate pH, improved water
holding capacity and better tenderness (Berri et al., 2007). There-
fore, a universal relationship between myofibre CSA and meat
quality still remains rather controversial. Because myofibre hyper-
trophy is a balance between protein synthesis and degradation, rel-
ative changes in both processes strongly affect myofibre growth
rate, as well as meat tenderization/tenderness through modulation
of p.m. proteolysis (Koohmaraie, Kent, Shackelford, Veiseth, &
Wheeler, 2002). At first glance, increasing TNF could be a good
strategy to simultaneously increase lean meat content while pre-
serving meat quality by reducing myofibre CSA. However, recent
cient, and that there would rather be a range of optimum TNF
which guarantees both high meat percentage and good meat qual-
ity at a moderate fibre size (Rehfeldt, Tuchscherer, Hartung, &
Kuhn, 2007). According to other studies, a high TNF combined with
a low percentage of type IIBW fibres would be a good strategy to
improve both lean meat content and meat quality in pig (Kim
et al., 2008; Ryu, Lee, Lee, & Kim, 2006).
264 L. Lefaucheur / Meat Science 84 (2010) 257–270
4.2. Fibre type composition
Because fibre type composition and meat quality can be dra-
matically different between muscles within the body, a possible
association between fibre type characteristics and meat quality
has been postulated. However, identifying the optimum fibre type
composition for best technological and sensory quality of meat re-
mains a challenge. Both the contractile and metabolic nature of fi-
bres likely influence meat quality. Thus, as previously presented in
the document (Table 1), fast-twitch glycolytic fibres exhibit a more
extensive and efficient SR, higher acto-myosin-ATPase activity, and
higher levels of glycogen than slow-twitch oxidative fibres which,
conversely, contain a higher number of mitochondria, as well as
more phospholipids and myoglobin. Consequently, according to
their composition in fibre types, muscles have different abilities
to release and sequester Ca2+, activate ATPase activities, produce
adenine nucleotides, stimulate glycolysis, produce lactate and de-
crease p.m. pH depending on their buffering capacity (Bowker,
Grant, Swartz, & Gerrard, 2004). Consistent with this, increasing
the proportion of fast-twitch glycolytic fibres (IIBW) in longissimus
muscle has been shown to increase the rate and extent of p.m. pH
decline, lightness (L*), paleness, cooking loss, protein denaturation,
and decrease water holding capacity in pigs (Choe et al., 2008;
Choi, Ryu, & Kim, 2006; Choi, Ryu, & Kim, 2007; Kauffman et al.,
1998; Larzul et al., 1997; Rosenvold et al., 2001; Ryu & Kim,
2005; Ryu & Kim, 2006; Ryu et al., 2008). However, other less
numerous studies have also reported that increasing the propor-
tion of fast-twitch oxido-glycolytic fibres decreased water holding
capacity of cooked meat, tenderness, juiciness and flavor (Henckel
et al., 1997; Maltin et al., 1997). Interestingly, a comparison be-
tween different pig muscles showed that the rate of p.m. pH de-
cline was much faster in the mixed psoas major than both the
slow-twitch oxidative semispinalis and fast-twitch glycolytic lon-
gissimus (Fig. 4), showing that rate of p.m. pH decline can depend
on other factors than fibre type composition, such as muscle buf-
fering capacity.
Post-mortem rate of maturation has been shown to be influ-
enced by fibre type composition. Thus, a study including different
muscles in cattle, pigs and sheep reported a higher calpain/calpast-
atin ratio in fast-twitch glycolytic than slow-twitch oxidative mus-
cles (Ouali & Talmant, 1990), which is consistent with the faster
p.m. rate of maturation in fast than slow muscles (Jurie, Robelin,
Picard, & Geay, 1995; Ouali, 1990). Therefore, increasing the pro-
portion of fast-twitch glycolytic fibres could have beneficial effects
on p.m. maturation and tenderness in species exhibiting slow p.m.
maturation, such as cattle (Seideman, Crouse, & Cross, 1986;
Zamora et al., 1996). This is in agreement with others results in cat-
tle showing a better tenderness in the superficial more glycolytic
than deep more oxidative region of semitendinosus muscle (Tot-
land, Kryvi, & Slinde, 1988). However, such correlations were not
I Semispinalis (S)
pH 24h
100
IIA Psoas major (P)
80 6.5 Longissimus (L)
IIB
60
% to be manipulated in conventional rearing conditions, i.e. genetic
40 6 factors, physical exercise, ambient temperature and nutrition.
20
0 5.5
S P L 45 min p.m. 24h p.m.
Fig. 4. Fibre type composition using conventional histochemical mATPase staining
after preincubation at pH 4.35 (left) and post-mortem pH (right) in semispinalis (S),
psoas major (P) and longissimus (L) muscles in the Large White pig. Lefaucheur
et al. (unpublished).
confirmed in other normal cattle breeds (Wegner et al., 2000) or
lambs (Solomon & Lynch, 1988).
Increasing the proportion of type I fibres has been reported to
decrease the rate and extent of p.m. pH decline and lightness,
and improve water holding capacity in pig (Choi et al., 2006; Gil
et al., 2003; Larzul et al., 1997; Ryu & Kim, 2005). Increasing the
proportion of slow-twitch type I fibres has been reported to im-
prove tenderness and juiciness in cattle (Maltin et al., 1998), and
juiciness and flavor in sheep (Valin, Touraille, Vigneron, & Ash-
more, 1982). The positive relationship between the proportion of
type I fibres and flavor is likely due to their high level of phospho-
lipids that have been shown to be major determinants of cooked
meat flavor (Meynier & Gandemer, 1994). However, the high levels
of polyunsaturated fatty acids in phospholipids also increase the
risks of p.m. fatty acid oxidation and development of rancidity.
Moreover, a high proportion of type I fibres is prone to the produc-
tion of dark, firm, and dry meat (DFD), in particular in beef meat
(Ozawa et al., 1999). It is also well documented that increasing
the proportion of type I fibres also decreases colour stability with
a possible shift to a brownish stain (Renerre, 1984).
Taken together, some relationships between fibre type compo-
sition and meat quality do exist but are not universal among spe-
cies and depend on numerous interacting factors such as muscle
type, species, breed, genotype, age, nutrition, environmental
factors, as well as slaughter conditions and p.m. processing. In
addition to myofibres, other muscle components such as intramus-
cular adipocytes and connective tissue can influence multiple
aspects of meat quality in an interconnected manner. Because of
this complex network of interactions, it is difficult to find a simple
and universal biological marker of meat quality that would be
usable in all situations. Rather, a better control of meat quality
needs a good understanding of muscle biology as a global complex
system submitted to the influence of multiple intrinsic and extrin-
sic factors.
5. Tools to control meat quality through fibre type composition
Muscle fibres are dynamic structures which exhibit high plas-
ticity and undergo type shift following an obligatory pathway
I M IIa M IIx M IIb (Pette & Staron, 2000; Schiaffino & Reggiani,
1994). Muscle histochemical characteristics can be influenced by
numerous intrinsic and extrinsic factors such as muscle location,
species, breed, genotype, gender, age, exercise, ambient tempera-
ture, nutrition, and growth promoting agents (Gondret, Combes,
Lefaucheur, & Lebret, 2005; Gunning & Hardeman, 1991; Pette &
Staron, 2001; Swynghedauw, 1986). Meat quality is also influenced
by many factors, among which the most important ones are re-
ported to be muscle location, species, pre-slaughter and slaughter
conditions, post-slaughter processing, genetic factors, growth
promoting agents, age and weight (Andersen, Oksbjerg, Young, &
Therkildsen, 2005; Dunshea, D’Souza, Pethick, Harper, & Warner,
2005; Ngapo & Gariepy, 2008; Rosenvold & Andersen, 2003;
Scheffler & Gerrard, 2007). Despite significant effects of some
growth promoting agents on both myofibre characteristics and
meat quality, this topic will not be presented in the present review
because the choice was made to focus on some factors susceptible
5.1. Genetic factors
Within species, muscle fibre type composition is strongly influ-
enced by genetic factors, such as breed, genotype and presence of
major genes. However, because differences between breeds are
also related to other factors than fibre type composition, i.e.
 L. Lefaucheur / Meat Science 84 (2010) 257–270
growth rate, body composition, and IMF content, these models are
not well suited to specifically address the relationships between
myofibre characteristics, growth performance, and meat quality.
This limitation is obvious for major genes presented in Table 2. In-
deed, they all induce an increase in carcass lean content, with var-
iable effects on TNF, myofibre CSA and fibre type composition not
directly related to differences in meat quality. Only the mutated
myostatin gene in cattle is associated with an additional increase
in TNF. On the opposite, increased muscle content of Ryr1 pigs is
exclusively related to increased myofibre CSA because they have
been shown to have either similar or reduced TNF. Morphologi-
cally, RN carrier pigs only exhibit an increased myofibre CSA of
fast-twitch oxido-glycolytic fibres. Interestingly, RN carrier pigs
also show increased glycogen level, AMPK and acetyl-CoA carbox-
ylase phosphorylations, AMPK activity, GLUT-4 expression at the
mRNA and protein levels, PGC-1a and FAT/CD36 mRNA levels in
longissimus muscle compared to wild type pigs (Park et al.,
2009), suggesting a greater reliance of glycolytic muscles on fatty
acid metabolism in mutated RN pigs. This is in accordance with
previous data showing an enhanced oxidative metabolism, CSA
and relative area of type IIA and IIBR oxydo-glycolytic fibres, and
a decreased glycolytic metabolism in longissimus muscle of RN
carrier pigs (Lebret et al., 1999). Even though total IMF content
of longissimus was not influenced by the RN genotype in this last
study, IMFL could have been decreased as shown in vastus lateralis
muscle of humans carrying the AMPK-c3 R225W mutation, which
also lead to a dramatic increase in muscle glycogen content (Cost-
ford et al., 2007). Taken together, most available data support a
negative correlation between IMFL and glycogen contents at the
myofibre level. Interestingly, additional mutated alleles in the
AMPKc3 gene with different effects on muscle glycogen content
have been discovered. Thus, the mutated V199I allele is correlated
with lower muscle glycogen and lactate, higher ham and loin pH,
and improved meat colour score, resulting in better meat quality
in pig (Ciobanu et al., 2001). From a practical point of view, manip-
ulations of these major genes are potential tools to control myofi-
bre development and meat quality in different species. In
particular, because of its central role (1) in vivo in the regulation
of systemic energy balance (food intake, glucose and lipid homeo-
stasis) and skeletal muscle metabolism (glycogen and IMFL con-
tents, energy metabolism), and (2) p.m. in its involvement in the
conversion of muscle to meat (Scheffler & Gerrard, 2007; Shen,
Gerrard, & Du, 2008; Underwood et al., 2007, 2008), AMPK appears
1.6
1.4
[gly co ge n], %
1.2
1.0
0.8
0.6
0.4
0.2
***
0.0
* IIBRIIBW
Low RFI IIA
High RFI I had to be stopped after the first generation of selection for sanitary
Fig. 5. Glycogen content of myofibres at 108 kg BW in longissimus muscle biopsies
of Large White pigs divergently selected for low and high residual feed intake (RFI).
Myofibres were classified as types I, IIA, IIBR and IIBW. *, P < 0.05; ***, P < 0.001.
Adapted from Lefaucheur et al. (2008).
265
50
40
Fiber number, %
30 *
20
**
10
0
I IIA IIBR IIBW
Fig. 6. Fibre type composition of triceps brachii muscle from sedentary (white bars)
and trained (black bars) miniature pigs. Animals were trained 5 d/week over 20
week. *, P < 0.05; **, P < 0.01). Adapted from McAllister et al. (1997).
to be a promising target to influence both myofibre characteristics
and meat quality.
Fibre type composition is highly variable between individuals of
the same breed reared under similar nutritional and environmental
conditions. Within the LW pig breed, the percentage of type I fibres
in the longissimus muscle ranges from 1.6% to 21.5% (9.5 ± 2.66,
CV = 28%), and mean myofibre CSA from 2560 to 6040 lm2
(3410 ± 620, CV = 18%) (Larzul et al., 1997). The TNF has also been
shown to be variable, ranging from 292  103 to 958  103
(533  103 ± 94  103, CV = 18%) in the semitendinosus muscle
within an F2 population of 364 LW  Meishan pigs (Lefaucheur
et al., unpublished). Muscle fibre traits exhibit moderate heritabil-
ities with h2 values ranging from 0.2 to 0.5 for TNF, 0.2 to 0.3 for
myofibre mean CSA, around 0.4 for fibre type frequencies, and
0.3 to 0.4 for glycogen in pig longissimus muscle (Larzul et al.,
1997, 1999; Oksbjerg, Henckel, Andersen, Pedersen, & Nielsen,
2004; Rehfeldt et al., 2000). As a comparison, average heritabilities
are 0.5 for carcass lean percentage, 0.5 for muscle IMF content, and
0.1–0.3 for meat quality traits, with 0.25–0.30 for colour and ten-
derness, and 0.15–0.20 for pH and water holding capacity (Sellier,
1998). The high individual variability of myofibre traits associated
to their moderate heritability makes it possible to select animals
directly on myofibre traits. This has been done for myofibre CSA
in pigs (Wicke, Von Lengerken, Fiedler, Altmann, & Ender, 1991);
however, results were flawed because of the indirect selection of
the mutated Ryr1 gene positively correlated with myofibre CSA,
but known to alter meat quality through another mechanism, i.e.
Ca2+ flux disregulation. A direct selection carried out for six gener-
ations against in vivo glycogen levels in longissimus muscle of LW
pigs free of the mutated Ryr1 and RN genes has been shown to in-
duce a decrease in carcass lean content and CSA of fast-twitch oxi-
do-glycolytic fibres, and improve meat technological quality
without any change in IMF content (Larzul et al., 1999). It is note-
worthy that correlated changes with this selection against muscle
glycogen content were consistent with the effects of the RN gene
on carcass lean content, muscle glycogen level, myofibre character-
istics and meat quality. The high heritability reported for the per-
centage of type I fibres in longissimus muscle (h2 = 0.46 ± 0.11)
(Larzul et al., 1997) led us to start a divergent selection on this
myofibre trait within the same population of LW pigs. Preliminary
results showed that divergent selection was effective from the first
generation (h2 = 0.29, 1.3 genetic standard deviation between the
two lines) (Lefaucheur et al., 2000). Unfortunately, this experiment
reasons unrelated to the selection experiment. At present time, a
divergent selection on residual feed intake (RFI) is under way
within the LW breed. After four generations, the animals from
the RFI-line, i.e. efficient animals, exhibited leaner carcasses and
lower longissimus IMF content (Lefaucheur et al., 2008). Moreover,
266 L. Lefaucheur / Meat Science 84 (2010) 257–270
RFI-pigs had a higher percentage of IIBW fibres, larger fibres, and
increased glycogen content, in accordance with a lower ultimate
pH and reduced water holding capacity. Interestingly, muscle gly-
cogen content increased specifically in type IIBW fibres (Fig. 5) and
further work is needed to identify the underlying mechanisms.
5.2. Exercise, ambient temperature and nutrition
Physical exercise is well known to influence myofibre charac-
teristics, depending on the type and duration of the exercise. Thus,
endurance exercise induces a IIBW ? IIBR ? IIA ? I transition in
muscles involved in the exercise. This has also been found in min-
iature pigs (Mcallister, Reiter, Amann, & Laughlin, 1997) (Fig. 6),
and confirmed in more conventional pigs, even though changes
were much weaker and probably not always of physiological
importance (Essén-Gustavsson, 1993; Petersen, Henckel, Oksbjerg,
& Sorensen, 1998). Long term cold exposure has been shown to
shift fibre type composition to a slower type in oxidative muscles
involved in posture in LW pigs (Herpin & Lefaucheur, 1992; Lefauc-
heur et al., 1991). At similar growth rates, an exposure to 12 °C vs.
28 °C between 8 and 92 kg BW also increased the rate and extent of
p.m. pH decline in longissimus, and enhanced the problem of bico-
lourism between muscles, which likely alter meat quality. On the
opposite, exposure to a warm environment has been reported to
decrease both oxidative and glycolytic metabolisms in pig glyco-
lytic muscles (Rinaldo & Le Dividich, 1991). Finally, 50% feed
restriction at thermoneutrality between 3 and 7 week of age did
not change fibre type proportions in longissimus muscle, whereas
it induced a 43% increase in the percentage of type I fibres in rhom-
boideus muscle, a red neck muscle (Harrison, Rowlerson, & Daun-
cey, 1996). Taken together, physical exercise, ambient temperature
and nutrition are potential tools which can be combined with ge-
netic factors (breed, genotype) in different rearing systems to con-
trol myofibre characteristics and meat quality.
6. Conclusion and future perspectives
The present review shows that some relationships do exist be-
tween myofibre characteristics and meat quality traits under given
conditions. Thus, in pig muscle, increasing the proportion and CSA
of IIBW fibres has often been shown to decrease water holding
capacity and tenderness. On the opposite, increasing the propor-
tion of type IIBW fibres has also been reported to improve meat
tenderness through improved p.m. maturation in cattle. As evi-
denced by the present review, there seems to be no universal rela-
tionship between myofibre characteristics and meat quality traits
among species because both traits are influenced by multiple fac-
tors such as species, breeds, genders, muscle location, sampling
sites within muscle, amount and nature of connective tissue and
intramuscular adipocytes, age, slaughter weight, degree of physio-
logical maturity at the time of slaughter, birth weight, myofibre
typing methods and methodology used to measure meat quality.
Thus, only a global approach including all parameters seems to
be pertinent to understand relationships between myofibre char-
acteristics, growth performance and meat quality.
The presence of four adult MyHC, i.e. I, IIa, IIx and IIb shows that
conventional enzyme histochemical classifications in three types,
i.e. I, IIA and IIB must be revisited, at least in species where IIb
MyHC is expressed such as pig, llama and rabbit. Fibre typing could
be ideally performed using specific monoclonal antibodies raised
against each MyHC. Unfortunately, such antibodies are not all
available and usable with the different immunological techniques
(immunocytochemistry, western blot, ELISA) in the different spe-
cies at different ages. The physical separation of all MyHC by elec-
trophoresis still remains a difficult task in meat producing animals
when IIb MyHC is expressed. Because measuring histological traits
is laborious and time consuming, identification of biochemical
markers of these traits would be a breakthrough. Unfortunately,
the identification of such markers remains elusive. Thus, poor cor-
relations between serum endocrine factor levels and muscle fibre
type composition have been found (Ryu, Choi, Ko, & Kim, 2007).
In the future, integrative techniques such as genomic, transcrip-
tomic, proteomic, and metabonomic could help to find such mark-
ers. So far, most significant advances have been done through the
identification of QTL but very few of them relate to myofibre char-
acteristics (Estelle et al., 2008; Nii et al., 2005; Wimmers, Murani,
Ngu, Schellander, & Ponsuksili, 2007), suggesting that myofibre
traits are under the control of multiple genes, in interaction with
environmental factors.
Numerous studies identified TNF as an important factor in-
volved in the control of both muscle growth and meat quality,
but its measurement remains a difficult task. Because TNF is fixed
before birth in most livestock animals, further work will have to be
done to study the influence of prenatal events on myogenesis. Due
to the high genetic variability and rather good heritability of most
myofibre traits, selection experiments directly based on myofibre
characteristics within breeds, and the study of correlated effects
on growth performance and meat quality parameters are promis-
ing ways to more specifically identify the relationships between
myofibre characteristics and meat quality. In addition to the
in vivo approaches, in vitro studies based on muscle cell cultures
should complete the experimental design to better understand
the mechanisms involved in the variability of TNF, myofibre CSA
and fibre type composition in meat producing animals. These
in vitro systems will be invaluable tools to study the regulation
of genes involved in the determination of fibre type characteristics,
such as those coding for myostatin and the different MyHC or those
involved in the AMPK network. The development and use of trans-
genic and knocked-out animals should also help to go further in
the understanding of muscle biology applied to meat production.
Of course, the achievement of these goals will need a multidisci-
plinary approach combining the competences of meat and animal
scientists, geneticists, biologists, physiologists, statisticians, and
mathematicians.
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