Avian Pathology

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Onset of white striping and progression into

wooden breast as defined by myopathic changes
underlying Pectoralis major growth. Estimation
of growth parameters as predictors for stage of
myopathy progression

Jacqueline Reedy Griffin, Luis Moraes, Macdonald Wick & Michael Snell
Lilburn

To cite this article: Jacqueline Reedy Griffin, Luis Moraes, Macdonald Wick & Michael Snell
Lilburn (2018) Onset of white striping and progression into wooden breast as defined by
myopathic changes underlying Pectoralis�major growth. Estimation of growth parameters
as predictors for stage of myopathy progression, Avian Pathology, 47:1, 2-13, DOI:
10.1080/03079457.2017.1356908

To link to this article: https://doi.org/10.1080/03079457.2017.1356908

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AVIAN PATHOLOGY, 2018
VOL. 47, NO. 1, 2–13
https://doi.org/10.1080/03079457.2017.1356908

ORIGINAL ARTICLE

Onset of white striping and progression into wooden breast as defined by

myopathic changes underlying Pectoralis major growth. Estimation of growth
parameters as predictors for stage of myopathy progression
Jacqueline Reedy Griffin, Luis Moraes, Macdonald Wick and Michael Snell Lilburn
Department of Animal Sciences, The Ohio State University, Columbus, OH, USA

ABSTRACT ARTICLE HISTORY

The broiler industry has incurred significant economic losses due to two muscle myopathies, Received 17 April 2017
white striping (WS) and wooden breast (WB), affecting the Pectoralis major (P. major) of Accepted 10 July 2017
commercial broilers. The present study documented macroscopic changes occurring with
KEYWORDS
age/growth in the P. major and P. minor muscles of commercial broilers from day 2 through Broiler; ontogeny; Pectoralis
day 46 (n = 27/day). Distinct myopathic aberrations observed in both breast muscles major; myopathy; white
corresponded to the onset of WB. These distinct morphological changes were used as striping; wooden breast
determinants in developing a ranking system, defining the ontogeny of WB as the following
four stages: (1) WS, (2) petechial epimysium haemorrhages, (3) intramuscular haemorrhages
and (4) ischaemia. A cumulative logit proportional odds model was used to relate the rank
probabilities with the following growth parameters: body weight, P. major and P. minor
weight/yield/length/width/depth. The best-fit model included P. major length/width/depth,
P. minor width, P. major and P. minor yield as predictors for rank. Increasing P. major depth,
P. minor width and P. major yield increased the odds of falling into higher ranks (more
severe myopathy). Conversely, increasing P. major length, P. major width and P. minor yield
increased the odds of falling into smaller ranks (less severe myopathy). This study describes
the macroscopic changes associated with WB ontogeny in the development of a ranking
system and the contribution of growth parameters in the determination of rank (WB
severity). Results suggest that physical measurements inherent to selection for high-yielding
broiler genotypes are contributing to the occurrence and severity of WS and WB.

Introduction
Darwin’s description of natural selection was substan-
tiated, in part, with the knowledge that humans had
successfully produced changes, over time, in domestic
animals using artificial selection (1859). For the broiler
industry, selection has remained focused on maximiz-
ing muscle growth for the production of meat (Barbut
et al., 2008). The Pectoralis major (P. major) and
M. supracoracoideus (P. minor) breast muscles are of
considerable value to the broiler industry, with the
P. major being the predominant meat producer and
consequently that of greatest economic value (USDA,
2016). As such, selection for increased P. major yield
has become a primary genetic focus of the broiler
industry, along with improvements in growth rate
and feed conversion (Havenstein et al., 1994, 2003;
Zuidhof et al., 2014). These improvements have led
to significant increases in body weight (BW),
P. major yield (Lilburn, 1994; Mazzoni et al., 2015)
and conformational changes in breast muscle (Godfrey
& Goodman, 1956; Reddish & Lilburn, 2004), resulting
in commercial strains that are marketed in half the
time with nearly twice the BW of their 1950s counter-
parts (Barbut et al., 2008). However, the same factors
integral to this success – a large decline in days to mar-
ket and disproportional increases in breast yield – have
contributed to an increase in skeletal muscle myopa-
thies (Petracci et al., 2015), such as Deep Pectoral
Myopathy (DPM), white striping (WS), wooden breast
(WB) and spaghetti meat (SM).
Among the first of these recognized myopathies is
DPM, identified as ischaemic necrosis of the P. minor
in broiler breeders (Page & Fletcher, 1975; Richardson
et al., 1980; Wight & Siller, 1980; Bianchi et al., 2006),
selected for increased breast muscle growth (Siller,
1985). Macro- and microscopic characterizations of
WS/WB have striking similarities to what have been
described for DPM (Wight et al., 1981), including mild
to severe oedema (Soglia et al., 2016), haemorrhagic/
inflammatory lesions (Sihvo et al., 2014; Bailey et al.,
2015; Trocino et al., 2015) and ischaemia (Kuttappan
et al., 2013a; Petracci et al., 2013a; Sihvo et al., 2014;
Zotte et al., 2014). Microscopic similarities include poly-
phasic degeneration, perivascular necrosis and infiltration
of connective and fat tissue (Kuttappan et al., 2012b; Kut-
tappan et al., 2013b; Kuttappan et al., 2013c; Ferreira et al.,
2014; Mudalal et al., 2014; Russo et al., 2015; Alnahhas
et al., 2016; Vignale et al., 2017; Zambonelli et al., 2016).

CONTACT Jacqueline Reedy Griffin griffin.347@osu.edu

© 2017 Houghton Trust Ltd

P. major breast muscles affected by WS and WB can
be easily distinguished from one another by their
macroscopic characterizations. WS is characterized
by the presence of white striations parallel to muscle
fibres (Kuttappan et al., 2009; Kuttappan et al.,
2012b), with varying degrees of haemorrhagic lesions
(Kuttappan et al., 2017), whereas WB is characterized
by a pale, hardened breast muscle with haemorrhagic
lesions (Sihvo et al., 2014), a condition that was first
detected in live broilers, as having palpably stiff breast
muscles (Puolanne, 2015). When examined histologi-
cally, the white striations and haemorrhagic lesions
associated with WS and the diffuse, hardened areas
associated with WB exhibit overlapping characteristics.
Included in these are: polyphasic myodegeneration,
perivascular necrosis, interstitial inflammation, perive-
nular infiltration of T lymphocytes with the infiltration
of connective tissue and lipid (Sihvo et al., 2014; Velle-
man & Clark, 2015; Abasht et al., 2016; Clark & Velle-
man, 2016; Baldi et al., 2017).
Lastly, a more recent muscular abnormality to be
reported in the P. major of modern broilers has been
termed SM, due to the altered structural integrity of
the P. major, characterized by poor fibre uniformity
(Baldi et al., 2017). Baldi et al. (2017) reported an
increase in P. major weight, thickness and length in fil-
lets affected by both WS and SM.
In addition to a correlation between WS and SM,
there are ample data to support an association etween
WS and WB (Sihvo et al., 2014, 2017; Bowker &
Zhuang, 2016; Tasoniero et al., 2016; Radaelli et al.,
2017). In addition, the onset and severity of each
anomaly are influenced by the same factors: Genotype
(high > standard breast yield) (Petracci et al., 2013b;
Alnahhas et al., 2016), gender (males > females) (Lor-
enzi et al., 2014), growth rate (fast > slow) (Kuttappan
et al., 2012a) diet (high > low energy) (Cruz et al.,
2017) and P. major weight (heavy > light) (Petracci
et al., 2014; Mutryn et al., 2015; Chatterjee et al.,
2016). Although these myopathies appear coincid-
ingly with one another, the cause-and-effect relation-
ships underlying their associations are not yet clear.
Not surprisingly, these myopathies have had a nega-
tive impact on consumer acceptability (Tasoniero et al.,
2016; Tijare et al., 2016), resulting in the downgrading
and condemnation of affected breast fillets. With
recent flock incidences (percent of broilers exhibiting
WS/WB) reported as high as 90% (Owens, 2016), the
industry has incurred significant economic losses,
with projections estimated to range from $200 million
to $1 billion (Owens, 2016).
Of greater concern, to the economic implications, is
the increasing welfare concern for those broilers exhi-
biting these myopathies; so the question becomes: at
what point does a meat-quality issue become a welfare
concern? Although the present study did not investi-
gate welfare parameters, this welfare concern is raised
AVIAN PATHOLOGY 3
as a direct result of the observations made in the pre-
sent study that led to its early termination two weeks
prior to the proposed end date. At 46 days of age, it
was determined unethical to maintain birds on feed
for further growth, as the vast majority exhibited severe
muscle damage (WS/ WB/ DPM) (details provided in
subsequent text).
In an effort to further understand the aetiology and
connection between these myopathies and their shared
characteristics, the overall objective of the present
study was to relate and characterize the muscle devel-
opment changes that occur with age/growth in the
P. major of commercial broilers beginning at day 2
post-hatch through 46 days post-hatch. During the
course of the experiment, distinct aberrations in the
macroscopic morphology of the P. major and
P. minor were observed corresponding to the onset
and progression of WB. In the present study, a ranking
system was devised to describe the ontogeny of WB
and a model was developed to relate the rank probabil-
ities with the physical measurements and growth par-
ameters associated with P. major and P. minor
growth during the post-hatch growth period.
Materials and methods
Experimental design
Birds, housing and management
All procedures involving the birds used in the present
experiment were approved by The Ohio State Univer-
sity Institutional Animal Care and Use Committee. A
mix of 1-day-old male and female commercial broiler
chicks (n = 900; Hubbard X Ross 708) was delivered
to the Ohio Agricultural Research and Development
Center (OARDC, Wooster, OH) Poultry Research
Farm. All chicks were wing-banded and randomly
placed in nine floor pens with feed and water available
for ad libitum consumption.
Sample collection
Broilers (three per pen/n = 27) were randomly sampled
on Monday, Wednesday, and Friday of each week from
2 to 46 days of age. Live BW was ascertained. Birds
were sacrificed via cervical dislocation, ensuring mini-
mal wing flapping. Immediately following cervical dis-
location, the intact P. major breast muscles were
exposed and photographed from top and side view-
points (see below). The subsequent sample procedures
were done in a sequential manner directly following
photo documentation. At this point, the left P. major
and P. minor muscles were immediately filleted and
individually weighed. [Weights were later used to cal-
culate P. major and P. minor yield as percentage of
live BW. In addition, relative growth was defined as
the percent change from the initial weight, set as 9
days of age (Actual-Initial/Initial × 100). Relative
4 J. R. GRIFFIN ET AL.
growth calculations were made using daily pen weight
averages for the three sampled birds and the data rep-
resent the average for all pens (n = 9)]. Immediately
after weight collection the depth of each muscle was
measured at the thickest point in the cranial region
of the muscle. At this point, both breast muscles were
placed on a ruler grid and fillets were photo documen-
ted for a second time for later use in obtaining geo-
metric measurements (length, width) using ImageJ
software (Schneider et al., 2012). P. major and
P. minor length were measured from the longest
dimension of the fillet and width from the two points
furthest apart from side to side (Kuttappan et al.,
2013a; Mudalal et al., 2014). To maintain consistency,
the same individual was responsible for filleting both
breast muscles, and obtaining muscle depth, length
and width measurements throughout the course of
the study.
Photo documentation
Image analysis (Photo documentation of both intact
superficial P. major muscles and filleted P. major and
P. minor breast muscles) began on day 16, following
the initial observation of physical changes to the
P. major. All photographs were obtained on an individ-
ual bird basis (n = 27 per day). Representative images
are shown in Figures 1–4. These images were later
used for assigning a rank (1–4) to individual birds,
representing their degree of progression from WS to
Figure 1. Rank 1 Pectoralis major breast muscle defined by the
presence of white striping (WS) only. WS severity was not
measured, although it is worth noting that breast muscles
with more apparent WS severity (increased thickness and
P. major coverage) exhibited same degree of haemorrhaging
or ischaemia and were therefore ranked accordingly.
WB. Rank 1 was defined by the presence of WS only
(WS severity was not measured) (Figure 1). All birds
exhibited some degree of WS following the initial
photo documentation, the reason for a lack of control
or completely unaffected muscle in the rank system.
Rank 2 is defined by the presence of surface (epimy-
sium) petechial haemorrhages (Figure 2). Rank 3 is
defined by intramuscular haemorrhages (bruising)
(Figure 3). Rank 4 is defined by ischaemia (loss of
blood supply observed as pale regions (Figure 4). As
WB is defined, in part, by pale regions of the
P. major breast muscle (Sihvo et al., 2014), rank 4
muscles were considered to have the WB myopathy.
Ranks 1–4 were established based on the sequential
onset of distinct myopathic abnormalities occurring
with increased growth/age. Based on the current litera-
ture, it was determined that ranks 1–4 depicted the
progression from WS to WB. In support of this con-
clusion, recent studies have reported an association
between haemorrhagic lesions and WS (Kuttappan
et al., 2017) and numerous studies (see Introduction)
have reported varying degrees of haemorrhaging and
ischaemia (pale regions) in WB-affected muscles
(Sihvo et al., 2014; Bailey et al., 2015; Trocino et al.,
2015; Soglia et al., 2016).
Once P. major myopathic abnormalities were
observed during the sampling process, palpable detec-
tion of live birds was conducted to assess the presence
of WB based on the established tactile method of WB
detection reported in the recent literature (i.e. hardness
of the breasts in live birds; Sihvo et al., 2014). The pre-
sent study outlines the sequential myopathic aberra-
tions associated with growth occurring in the
Figure 2. Rank 2 Pectoralis major breast muscle defined by sur-
face (epimysium) haemorrhaging near the sternal apex.

Figure 3. Rank 3 Pectoralis major breast muscle defined by
intramuscular haemorrhaging (bruising) near the sternal apex.
P. major, to elucidate the underlying morphological
changes occurring at earlier ages, prior to the point at
which WB can be detected in live birds. Therefore,
the present study reports the first day in which WB
was first detected using these same tactile methods
(Sihvo et al., 2014), but did not intend to use this
method to characterize WB severity, as the first-day
detection was not conducted until day 42.
Figure 4. Rank 4 Pectoralis major breast muscle defined by
ischaemia (extreme paleness) near the periphery regions of
the muscle.
AVIAN PATHOLOGY 5
Statistical analyses
The initial exploratory analysis of the data investigated
rank (P. major myopathy progression) differences on
growth parameters, using a linear mixed effects model.
In particular, the PROC MIXED of SAS v. 9.4 was
used to test for differences in growth parameters
among ranks, using a model with fixed effect of rank
and random effect of pen. The second step of the data
analysis focused on understanding the contributions of
specific growth parameters in the determination of
ranks. A generalized linear mixed model was used to
examine the effect of growth parameters on the rank
probabilities. A cumulative logit link function was used
in a proportional odds model (Stroup, 2013) with a ran-
dom intercept for pens and fixed regression coefficients
for growth parameters. The selection of growth par-
ameters to be used as subsequent predictors was con-
ducted using the following sequential steps: (i) all
possible models were created with all possible combi-
nations of the independent variables (P. major length,
P. major width, P. major depth, BW, P. major
weight, P. minor weight, P. minor length, P. minor
width, P. minor depth, P. major yield and P. minor
yield); (ii) models for which the variance inflation factor
was greater than 10 were discarded; (iii) all remaining
models were fitted to the data; (iv) the 10 models with
the smallest Akaike Information Criterion (AIC) were
selected for further examination and (v) the model
with the smallest AIC was used for biological inference.
Both the ordinal R package (Christensen, 2015) and the
PROC GLIMMIX procedure of SAS v. 9.4 were used for
model selection and fitting.
Results
Age- and growth-associated myopathic
aberrations
Based on the progressive changes and abnormal
clinical presentation observed during P. major post-
hatch growth, the present study developed an objec-
tive ranking system which defined the onset and
progression of WB. Relative growth rate and relative
growth changes in the weight of the P. major and
P. minor are presented in Figure 5. The distinct myo-
pathic changes associated with age and relative
growth are indicated on the day in which they were
initially observed (Figure 5), starting with the onset
of WS on day 16. On day 18, was the initial onset
of SM and surface (epimysium) petechial haemor-
rhages followed by deep intramuscular haemorrha-
ging (bruising) on day 21.
SM myopathy has been previously shown to be associ-
ated with WS (Baldi et al., 2017). In the present study, the
initial onset of SM occurred after (day 18) the initial onset
of WS (day 16) and coincided with the initial onset of epi-
mysium haemorrhages. Throughout the remainder of
6 J. R. GRIFFIN ET AL.
Figure 5. Relative growth rate and relative growth changes in P. major and P. minor breast muscles ([Actual weight−initial weight
(day 9)]/initial weight (day 9) × 100). Grossly observed myopathic changes associated with age and relative growth are indicated
above the day in which they were initially observed. WS = White striping WB = Wooden breast DPM = Deep pectoral myopathy.
the study and after a thorough study of the numerous
photographs over the course of the experiment, it became
clear that the occurrence of the SM myopathy was highly
variable among birds and often difficult to detect visually
in the photographs. In contrast, epimysium haemorrha-
ging progressed in a consistent pattern with growth/age.
Given the nature of the study, and the aim to objectively
define ranks, for these reasons, SM was not included as a
rank determinant. However, the timing of SM onset, rela-
tive to WS and WB, could perhaps prove useful in sub-
sequent studies.
Lastly, the first documented case of WB (i.e. rank 4)
was noted on day 23 and was characterized as a
P. major muscle that was extremely pale in colour
with a ridge-like bulge on the caudal end. More severe
cases of WB were observed from day 30 onwards and
included prominent changes in muscle shape (firm
and flat with a prominent ridge on the caudal end),
interstitial viscous fluid accumulation and severe hae-
morrhaging (surface and intramuscular). In the most
severe cases, affected muscles were completely void of
vascularization throughout the entire P. major muscle
with a thick, viscous yellow interstitial exudate sur-
rounding the muscle. Other characteristically severe
cases included breast muscles that were nearly comple-
tely covered with thick white striations (WS), displa-
cing the surrounding epimysium with a thick
collagenous layer, some with extreme haemorrhaging,
where the white striation coverage was largely red in
colour due to the extent of petechial haemorrhaging
associated with the WS.
The most common method reported amongst the
literature for detecting WB is via palpable detection
of stiff breast muscles in live birds. As such, the
present study aimed to determine the day in which
live detection was first possible. Using tactile
methods, WB was first detected in live broilers on
day 42. As mentioned previously in Materials and
methods, it was not the intention of the present
study to utilize this method as a means to detect
WB severity, as the majority of birds by this age
exhibited mild to severe myopathies (rank 3 and 4).
Rather, the intention was to determine the age at
which live detection was possible for relative com-
parisons to the underlying aetiology of myopathic
progression occurring in the P. major reported herein.
As shown in Figure 5, the P. minor and Gastrocne-
mius muscles underwent similar myopathic changes
during later stages of growth, starting with the initial
observation of WS on day 32. The first reported case
of DPM in the P. minor was on day 35. Lastly, on
day 46 the P. minor exhibited WB-like abnormalities
(i.e. rank 4), as a grossly pale muscle with a ridge-like
bulge at the caudal region.
The muscle changes leading to the onset of WB
occurred in a cumulative manner paralleling their
progression with age/growth. Birds exhibiting surface
epimysium haemorrhages (rank 2) also exhibited
varying degrees of WS (rank 1). Furthermore,
muscles exhibiting deep intramuscular haemorrhages
(rank 3) also exhibited surface haemorrhages (rank
2) and WS (rank 1). Lastly, ischaemic muscles
(rank 4) exhibited intramuscular (rank 3) and surface
(rank 2) haemorrhages, as well as varying degrees of
WS (rank 1). Given this progressive pattern, these
distinct changes were used as markers for each
rank. Representative images from each rank group
are shown in Figures 1–4.
 AVIAN PATHOLOGY 7

Image quality rank determinants later diffusing throughout the entire muscle. Although
not used as a determinant for rank 4 classification, it
Rank 1 is classified by the presence of WS. On day 16,
should be noted that in conjunction with the onset of
faint white striations were observed in the cranial
ischaemia, there were observable changes in shape,
region of the P. major, present beneath the surround-
which included a flat, ridge-like bulge on the caudal
ing fascia (epimysium). By day 21, striations were easily
end of the P. major. These data are in agreement
seen on the P. major surface as part of the surrounding
with the current literature, which partially defines
epimysium. Throughout the remainder of the study,
WB by the presence of a pale ridge-like bulge (Sihvo
WS was no longer limited to the cranial region of the
et al., 2014; Trocino et al., 2015; Soglia et al., 2016).
P. major but had infiltrated the entire P. major muscle.
It is also reported to be lighter in colour when com-
This progressive infiltration coincided with an increase
pared to normal breast fillets (Kuttappan et al.,
in WS thickness (Figure 1). These data agree with
2013a; Petracci et al., 2013a).
authors who have grossly classified the severity of
WS as an increase in striation number and size (Kut-
tappan et al., 2012b), initially limited to the cranial Image rank frequency and growth parameters
region and subsequently developing caudally in the by day
P. major (Kuttappan et al., 2013c).
As previously mentioned, the occurrence and severity
Rank 2 is classified by the presence of surface (epi-
of WS/WB is positively correlated with increased
mysium) haemorrhages which was initially observed
growth rate (Kuttappan et al., 2012a). As such, rank
on day 18. Epimysial haemorrhages were initially
frequency, as a percentage of total birds, was calculated
small and focalized near the sternal apex, where visible
on each day to show the distribution of rank (1–4) with
stretching of the epimysial sheath could be seen.
age and growth (Figure 6). A clear trend from lower to
Throughout the course of the study, haemorrhages
higher ranking (less to more severe myopathy) can be
increased in size and dispersed throughout the
observed with age/growth from day 18 through day
P. major muscle (Figure 2). These data agree with
46 (Figure 6). In addition, individual growth data
studies that have reported P. major surface haemor-
(without rank separation) were plotted by day, to
rhages associated with varying severity of WB (Sihvo
show growth trends over time (Figure 7).
et al., 2014; Bailey et al., 2015).
The overall objective of the present study was to
Rank 3 is classified by the presence of deep intra-
relate the rank probabilities (stage/severity of WB)
muscular haemorrhaging (bruising), initially observed
with physical measurements associated with P. major
on day 21 (Figure 3). Similar to the progression
and P. minor muscle growth and development. In
described for rank 2, intramuscular haemorrhages
order to ensure differences in growth among the
were initially present near the sternum apex, dispersing
ranks, multiple least square mean comparisons for
distally throughout the P. major with age/growth. This
growth parameters were performed with respect to
coincided with an increase in colour intensity (red and
rank group (1–4). Significant differences (P < 0.001)
purple). This is in agreement with studies that have
were shown for all growth parameters investigated
characterized WB by the presence of large haemorrha-
among ranks. The variation in BW and muscle data
gic foci (Trocino et al., 2015).
(P. major and P. minor weight, yield, length, width,
Rank 4 is classified by the presence of extreme pale-
depth) among ranks 1–4 are presented in Figure 8 as
ness (ischaemia), initially observed on day 23,
individual boxplots. Mean rank values are denoted
coinciding with the first documented case of WB
above respective rank boxes and differing superscripts
(Figure 4). Ischaemia was initially present in the per-
signifying least square mean separation are denoted
ipheral regions of the P. major muscle at earlier ages,
between each sequential rank (P < 0.001).

Cumulative logit model

Figure 6. Image rank (1–4) frequency by day. Rank percentage
is based on total birds for each respective day.
In order to understand the contributions of specific
growth parameters in the determination of ranks
(WB ontogeny), a cumulative logit mixed model was
developed to determine the role of one or more growth
attributes as predictors for the probability of breast fil-
lets being assigned to the four ranks. The 10 best (i.e.
smallest AIC) cumulative logit mixed models with pro-
portional odds are presented in Table 1, with inter-
cepts, parameter estimates and standard errors given
for all 10 best-fit models. Within each model, odds
ratios were determined for individual predictors
8 J. R. GRIFFIN ET AL.

Figure 7. Boxplots display individual growth parameter data over age, starting on day 25 through day 46. Boxes indicate the range
of data values between the first and third quartiles (25th and 75th percentiles); intra-quartile range (IQR). Whiskers extending from
each box indicate range of data outside the IQR, ending with minimum and maximum data points. Within each box, lines (▬)
represent day averages and circles (●) represent outlier data points.

while holding all other predictors at a constant value.
The model which best fit the data (Model 1) included
the following growth parameters as predictors for
rank: P. major length, P. major width, P. major
depth, P. minor width, P. major yield and P. minor
yield. For the best fit model (Model 1), the odds ratios
showed that increasing P. major depth, P. minor width
and P. major yield increased the odds of the muscle
falling into a higher rank (i.e. more severe myopathy)
versus a lower rank (less severe myopathy). In other
words, increasing these muscle factors increased the
likelihood of them having a higher rank (i.e. increased
progression and severity of WB). Conversely, increased
values for P. major length, P. major width and P. minor
yield increased the odds of these muscles falling into
lower ranks (less severe myopathy) versus a higher
rank (more severe myopathy). In other words, increas-
ing these muscle factors decreased the likelihood of
them having a higher rank.
In considering the top 10 best models shown in
Table 1, P. major depth, P. major yield and P. minor
yield were included as predictors for rank in all of
the 10 best-fit models. P. major width was present in
8 of the 10 best models and P. major length was present
in five of the 10 best models. P. minor width was pre-
sent in seven of the 10 best models.
 AVIAN PATHOLOGY 9

Figure 8. Boxplots show descriptive growth parameter data for individual ranks 1–4. Boxes indicated data values falling within the
Intra-quartile range (IQR) between the first and third quartiles (25th and 75th percentiles). Whiskers extending from each box indi-
cate range of data outside the IQR, ending with minimum and maximum data points of each growth parameter. Within each box,
lines (▬) indicate rank median and circles (●) indicate rank means. Mean values are denoted above their respective rank boxes and
differing superscripts indicate significant differences in least square means among ranks (* = P < 0.001).

Discussion damage resulting from this was surface haemorrhaging

present on the epimysium only (rank 2). With advan-
The present study characterized the macroscopic phe-
cing age and increased muscle growth, intramuscular
notypic muscle traits of the P. major and P. minor cor-
haemorrhages (rank 3) were observed in regions with
responding to the ontogeny of WB in commercial
prominent surface haemorrhaging (near the sternal
broilers and developed a rank score system based on
apex). It is hypothesized that the continued increase
these distinct traits. It is generally accepted that during
in the degree and depth of the haemorrhages further
the onset of WB there is an inflammatory response, the
decreased intramuscular blood flow, leading to ischae-
cause of which is still unknown. In the present study,
mia (rank 4).
the first abnormality observed during post-hatch
A cumulative logit model was developed to try and
growth was the appearance of WS (fat/connective tis-
understand the morphological components of muscle
sue) on day 16. As the muscle increased in size with
growth that contributed most to the ranking system
age, the WS striations were observed close to the sur-
described in this report. The model that best fit the
face of the P. major and ultimately became part of
data showed that an increase in P. major depth and
the surrounding epimysium (rank 1). The primary
P. major yield increased the odds of that breast muscle
10 J. R. GRIFFIN ET AL.

exhibiting a more severe stage of WB (i.e. higher rank).

1.54 (0.53)
1.50 (0.53)
1.72 (0.56)
1.67 (0.53)
1.45 (0.53)
1.32 (0.48)
1.18 (0.50)
1.39 (0.58)
1.61 (0.58)
1.52 (0.54)
Yield
Alternatively, the predictors P. major width and
P. major length were shown to be inversely related to
the severity of WB. These data are in agreement with

−0.487 (1.54)
studies that reported an association between WS and

Depth
–
–
–
–
–
–
–
–

–
WB and P. major depth (Kuttappan et al., 2013a;
Mudalal et al., 2014) as well as P. major yield (Petracci
Table 1. The 10 best (i.e. smallest AIC) cumulative logit mixed models with proportional odd estimates for growth parameters determined to be predictors for myopathy rank.

et al., 2013b; Alnahhas et al., 2016). Among these

−1.72 (0.83)
−1.71 (0.83)
−1.52 (0.81)
−1.84 (0.85)
−1.36 (0.81)
−1.73 (0.84)

−1.74 (0.84)
P. minor

reports, Kuttappan et al. (2013b) measured P. major

Width

–
–
–
length, width and depth and reported an association
between the occurrence of WS and P. major depth,
only (Kuttappan et al., 2013a; Kuttappan et al., 2017).
0.296 (0.27)

0.073 (0.35)
Length

Furthermore, Mudalal et al. (2014) reported signifi-

–
–
–
–

–
–
–
–
cantly greater P. major depth values in WS/WB-
affected fillets, with no differences in fillet length or
0.008 (0.01)

width (Mudalal et al., 2014).

Weight

The current data further support a hypothesis that

–
–
–
–
–
–
–

–
–

by increasing P. major length and width, the odds of

falling in a higher rank (more severe myopathy) are
Body Weight

actually decreased. The contrasting relationships

between selected phenotypic muscle measurements
and the severity of WB confirms the fact that physical
–
–
–
–
–
–
–
–
–
–

measurements which are inherent to selection for high-

−0.70 (0.18)
−0.671 (0.19)

−0.771 (0.19)
−0.598 (0.18)
−0.668 (0.19)
−0.575 (0.18)
−0.645 (0.18)
−0.687 (0.19)
−0.684 (0.19)
−0.669 (0.19)

yielding broiler genotypes are contributing to the

Yieldb

occurrence and severity of the observed myopathies.

The growth of the P. minor as a predictor for rank is
also of interest, particularly due to the inverse relation-
0.005 (0.004)
Weight

ship between P. major and P. minor yield and rank. The

–
–

–
–
–
–
–
–
–

best fit model for predicting rank indicated that an

increase in P. minor yield would decrease the odds of
a higher rank (more severe WB) whereas increasing
−4.69 (0.93)
−4.23 (0.86)
−5.10 (1.10)
−4.64 (0.93)
−4.56 (0.92)
−4.96 (0.91)
−4.64 (0.83)
−4.50 (1.01)
−4.50 (1.08)
−4.70 (0.93)
P. major
Depth

P. major yield increased the odds of higher rank.

These data, in conjunction with the physical measure-
ment data, suggest that alternate selection strategies for
0.741 (0.323)

optimizing growth rather than maximizing it might be

0.815 (0.39)

0.861 (0.39)

0.953 (0.39)
0.685 (0.44)
1.04 (0.36)

0.703 (0.43)
0.687 (0.43)
Width

considered when trying to genetically minimize these

–

growth-associated muscle anomalies.

It has been hypothesized that in poultry selected for
0.335 (0.231)

meat production, growth of the epimysium can no

0.537 (0.19)

0.407 (0.17)
0.329 (0.23)

0.287 (0.30)
Length

longer keep pace with underlying muscle growth, lead-

–
–

–
–

ing to the onset of muscle damage (Swatland, 1990; Kra-

nen et al., 2000) Observations from the present study
(1.60)
(1.09)
(1.16)
(1.03)
(1.00)
(1.45)
(1.15)
(1.12)

(1.16)
(1.16)

provide evidence in support of that hypothesis – that

Rank 3

the breast muscle has outgrown its surrounding epimy-

10.3
7.91
8.47
7.33
7.95
9.32
8.44
8.84

8.43
8.41

sium. It is likely that accelerated muscle growth reduces

(1.00)
(0.96)
(1.42)
(1.12)
(1.08)
(1.56)
(1.06)
(1.13)

(1.12)
(1.13)

the interstitial space between the P. major muscle and

Intercept
Rank 2

its surrounding epimysium, limiting subfascial move-

6.06
6.62
5.49
6.11
7.47
6.58
6.99
8.46

6.58
6.56

ment in response to normal physiologic stimuli (move-

ment, wing flapping, etc.), leading to muscle damage. In
4.92 (1.08)
5.34 (1.05)
6.80 (1.54)
4.42 (1.04)
4.96 (1.10)
3.85 (0.98)
4.47 (0.93)
5.82 (1.39)
4.92 (1.09)
4.90 (1.11)
Akaike Information Criterion (AIC).
Rank 1

Percentage of live body weight.

the P. minor, the consequences of such fascial inelasti-

city (DPM) result in a rise in intramuscular pressure
(IMP), ischaemia, hypoxia and eventual necrosis (Mar-
Model 10 (AIC = 731)
Model 1 (AICa = 729)
Model 2 (AIC = 729)
Model 3 (AIC = 729)
Model 4 (AIC = 729)
Model 5 (AIC = 730)
Model 6 (AIC = 730)
Model 7 (AIC = 730)
Model 8 (AIC = 730)
Model 9 (AIC = 731)

tindale et al., 1979), of which, the onset of ischaemia is

prevented experimentally by cutting the surrounding
epimysium (fasciotomy) (Martindale et al., 1979).
DPM in the P. minor exhibits striking similarities in
appearance and potential growth limitations by the
b
a

surrounding epimysium to WB in the P. major. The
most obvious difference was the grossly observed yel-
low/green necrotic muscle associated with DPM in
the P. minor. When consideration is given to the differ-
ences in confounding factors between the P. minor
(surrounding epimysium, sternum and overlaying
P. major muscle) and P. major (surrounding epimy-
sium), it is possible that WB represents simply a slower
progression of DPM that is now manifest in the
P. major as a result of continued selection for increased
muscle mass. There are thus significantly less pressure-
inducing factors confounding the P. major, preventing
it from exhibiting necrosis phenotypically analogous to
DPM in the P. minor.
DPM occurs as a result of increased IMP, limited by
the space within the surrounding epimysium. In the
present study, an increase in P. major depth and
P. major yield was the primary predictor for WB pro-
gression or rank, suggesting that an increase in IMP
may be a contributing factor in the progression of
WB. Furthermore, several studies have reported the
spatial morphological effect on the degree of WS/WB
severity. In particular, the anterior cranial end of the
P. major has been reported to be more severely affected
by these conditions (Bowker & Zhuang, 2016; Clark &
Velleman, 2016). In addition, WB is initially palpable
in the anterior region of the P. major in less-severe
cases, but progresses throughout the entire fillet in
severe cases (Bailey et al., 2015; Soglia et al., 2016).
Soglia et al. (2016) reported a clear and gradual
decrease in histopathological lesions from the
P. major surface towards the inside of the P. major.
It is important to consider the repercussions of
long-term changes resulting from 50 years of focused
quantitative trait selection for increased breast muscle
mass (yield). The substantial economic losses result-
ing from recent muscle myopathies provide a unique
opportunity for the industry to re-evaluate current
selection strategies and aim towards alternative sus-
tainable solutions, focused on optimizing growth
rather than maximizing it. Such considerations are
critical to ensuring a sustainable future for the broiler
industry, on an economic, environmental and social
level.
Acknowledgements
Grateful acknowledgements are given to the following
OARDC Chicken Research Facilities staff:Keith Patterson,
Jordan Welsh and Jarrod Snell. Their support and enthu-
siasm during frequent and time-consuming data collections
made this research possible.
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