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PROCESSING AND PRODUCTS

Roaster Breast Meat Condemned for Cyanosis:


A Dark Firm Dry-Like Condition?

J. G. Mallia,* S. Barbut,† J.-P. Vaillancourt,‡ S. W. Martin,* and S. A. McEwen*,1

*Department of Population Medicine, †Department of Animal & Poultry Science, University of Guelph, Guelph, Ontario,
Canada N1G 2W1; and ‡Department of Food Animal and Equine Medicine, North Carolina State University,
Raleigh, North Carolina 27695-7608

ABSTRACT A case-control study (n = 68) of roaster (a*) at slaughter time and after 24 h. Ultimate pH and
chickens condemned for cyanosis was conducted. Color lightness at 24 h postmortem were also correlated. Tests

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(CIE L*a*b*) and pH were measured at slaughter, and based on pH, L*, and a* of the P. major were assessed:
after 24 h aging on ice, at four predetermined sites of the sensitivity and specificity at various cut-off points
the Pectoralis major. Cyanotic carcasses (dark) had a were, respectively, pH(6.3) = 76.47 and 88.24%, L*(41) =
91.18 and 79.41%, and a*(3) = 76.47 and 97.06%. The
higher pH than controls at the time of slaughter and at
repeatability (ρ) of pH and color measurements was ex-
24 h postmortem (P < 0.01). Perimortem pH was signifi- cellent and ranged from 0.87 to 0.98. Breast meat from
cantly correlated with pH at 24 h postmortem (r = 0.64) roasters condemned for cyanosis had dark, firm, and
and also was correlated with lightness (L*) perimortem dry (DFD)-like traits, and accurate tests based on color
and postmortem (24 h; r = −0.36 and −0.50, respectively). and pH could be described as a means of identifying
Perimortem pH was not correlated with meat redness chickens condemned for cyanosis.
(Key words: broiler, dark firm dry, cyanosis, poultry color, texture)
2000 Poultry Science 79:908–912

INTRODUCTION ever, the dark coloring of cyanotic birds was suggested


to be a problem related to shipping stress (Mallia, 1998).
Cyanosis is a category of condemnation adopted by Shipment and other stressors occurring prior to slaugh-
Agriculture and Agrifood Canada (AAFC) to describe ter are believed to be responsible for the occurrence of
poultry with a dark-colored carcass and no other condem- dark, firm, and dry (DFD) conditions in other species
nable lesions. Cyanosis was the fourth leading cause of (Tarrant, 1989; Swatland, 1994; Apple et al., 1995; Nielsen,
condemnation of chickens in Canada in 1993 and 1994, 1981). The DFD meat has a higher pH, as has been shown
representing almost 10% of all condemned chickens (Her- in swine (Bendall and Swatland, 1988) and cattle (Tarrant,
enda and Franco, 1996); roughly one million chickens 1989). A DFD-like condition has also been observed in
were condemned for cyanosis in this period. Therefore, ducks (Chen et al., 1991) and turkeys (Mallia et al., 1996).
there is a strong interest to fully assess the situation and The presence of DFD meat in other poultry appears some-
to examine the suitability of cyanotic carcasses for fur- what contradictory. Walker and Fletcher (1993) indicated
ther processing. that meat from chickens subjected to stressors was darker
and had a higher pH than meat from unstressed birds,
Cyanotic meat is currently condemned because little is
suggesting a stress-related DFD-like condition. In con-
known about its safety and quality. It has been suggested
trast, the results of several other studies that examined
that environmental conditions producing chronic hyp-
the relationship between meat color and pH do not sup-
oxia, such as those observed in overcrowded poultry
port the presence of a DFD-like condition in inspected
crates, favor the occurrence of cyanosis (Herenda and
poultry meat (Froning et al., 1978; Wyers et al., 1992;
Franco, 1996). This cause has neither been confirmed nor
Boulianne and King, 1995; Papinaho et al., 1996).
disproved by research, as contradictory evidence has been
Concerns have been expressed over the lack of stan-
obtained (Sackett et al., 1986; Boulianne et al., 1993). How-
dardization of condemnation criteria for cyanosis in
chickens. Poor diagnostic agreement for chickens con-

Received for publication February 19, 1999.


Accepted for publication February 23, 2000. Abbreviation Key: AAFC = Agriculture and Agrifood Canada; DFD
1
To whom correspondence should be addressed: smcewen@ = dark, firm, dry; PSE = pale, soft, exudative; SE = sensitivity; SP = speci-
uoguelph.ca. ficity.

908
CYANOSIS IN ROASTER BREAST MEAT 909
demned for cyanosis was reported in a previous study mysium was left intact. Color measurements on each site
examining different condemnable conditions (Bisaillon et were performed within 15 s of the skin removal. Chroma-
al., 1988), suggesting that the postmortem visual examina- ticity was measured using the color coordinates of the
tion at the abattoir may be deficient in some respects. Commission Internationale de l’Eclairage (CIE, 1976) for
Other tests may, therefore, be of practical use to the indus- L* (lightness), a* (redness), and b* (yellowness), under
try if they improve the identification of cyanotic carcasses. the CIE illuminant C lighting condition. After initial mea-
For example, it may be possible to use colorimetry to surements, the P. major was excised, weighed, and stored
objectively measure color and thereby identify cyanotic on ice at 4 C for 24 h. Color measurements were then
carcasses, as this method is already used to detect other repeated in an identical fashion.
commercially important meat conditions such as pale,
soft, exudative (PSE) and DFD meat in pork and beef Muscle pH
(Swatland, 1989).
The main objectives of this study were 1) to investigate A probe3 was used to measure the pH of the P. major
the presence of a DFD-like condition in roaster chickens at the same four sites utilized for the color assessment.

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condemned at slaughter as “cyanotic,” and 2) to evaluate After adjusting for muscle temperature, the pH was re-
the ability of pH and colorimetric tests to differentiate corded (at a depth of 1 cm) when a stable reading was
cyanotic carcasses from those that passed inspection. observed for 10 s. The same four muscle sites were used
for ultimate pH measurements, after storage on ice for
MATERIALS AND METHODS 24 h.

Study Design and Sample Size Statistical Analyses


Sixty-eight 8-wk-old male chickens (roasters) submit- A McNemar’s t-test was used to assess the difference
ted to a single abattoir in southern Ontario over a 3-wk among means of the two groups as the data were paired.
period were evaluated in a case-control study conducted Four simultaneous parameters were assessed (pH, L*, a*,
in November 1996. Conventional electrical stunning and b*) on the same sample of each carcass. To keep the Type
a hot water subscald (soft scald) were used. A case (n = I error level to 5%, the Bonferroni approach to control
34) was defined as a roaster carcass condemned by the the overall level of significance was used (Shoukri and
veterinary inspector for cyanosis, and a control (n = 34) Edge, 1996). Pearson’s correlation coefficients were used
was the next fifth carcass that passed the inspection proce- to assess linear correlations between pH and L*, a*, or b*
dure. All carcasses condemned for cyanosis during a rou- (Snedecor and Cochran, 1980). The intraclass correlation
tine inspection were independently examined by the se- coefficient for color and pH was based on four different
nior author (a veterinarian) to ensure correct classification sites of the P. major and was performed to assess the
prior to inclusion in the study. The examination consisted repeatability of color (L*, a*, b*) and pH. The ANOVA
of a necropsy that evaluated the general appearance of estimator of the intraclass correlation coefficient (ρ) was
the carcass, the coelom, and viscera for grossly evident calculated using the one-way random effects model
pathological lesions. The roasters were raised on various (Fleiss, 1986), and the time-lag was accounted for by the
farms in Southern Ontario and were of similar age, sex, use of a correction factor suggested by Stanish and Tay-
and general characteristics to those raised across Ontario. lor (1983).
The sensitivities (Se) and specificities (Sp) of the pH,
Muscle Color L*, and a* tests were established for the identification of
cyanotic carcasses, at different cut-off points. Sensitivity
The color of four specific sites of the ventral aspect of was defined as the probability that a truly positive sample
the right Pectoralis major was measured2 within 20 min will test positive, and Sp was defined as the probability
of slaughter without the removal of the overlying skin, that a truly negative sample will test negative (Martin et
as occurs visually during commercial inspection. The skin al., 1987). The coefficient of reliability K (ρ2) of the pH,
was patted dry with a paper towel prior to color evalua- L*, and a* tests was also assessed (Tenenbein, 1970).
tion. The specific sites chosen included 1) the proximal Agreement among the pH test, L* test, and a* test was
extremity of the muscle, 2) the distal extremity of the measured by the use of Cohen’s kappa statistic, κ (Cohen,
muscle, 3) the medial side at the half-way point between 1960), divided into categories as defined by Landis and
the proximal and distal extremities, and 4) the lateral side Koch (1977). This test measures the degree of agreement
at the half-way point between the proximal and distal beyond chance.
extremities. Later, the skin overlying the breast muscle
was removed, and the intact muscle was patted dry with
RESULTS
a paper towel prior to color evaluation; the muscle peri-
The color and pH differences between cases and con-
trols at time of slaughter and 24 h postmortem are shown
2
Chroma Meter CR-200b, Minolta, Osaka 541, Japan. in Table 1. Cyanotic carcasses were significantly darker
3
pH Stickmeter, Fisher Scientific, Nepean, ON, Canada, K2E 7L6. and redder than controls at the time of slaughter; they
910 MALLIA ET AL.
TABLE 1. Pectoralis major characteristics of roasters condemned for cyanosis and control

0.5 h 24 h
Cyanosis Control2,3 Cyanosis2 Control2,3
Parameter1 (n = 34) (n = 34) P-value4 (n = 34) (n = 34) P-value4
L* 38.36 ± 0.33 41.66 ± 0.33 ≤0.05 41.87 ± 0.55 47.49 ± 0.34 ≤0.01
a* 4.72 ± 0.16 2.48 ± 0.14 ≤0.05 4.51 ± 0.20 2.21 ± 0.13 ≤0.01
b* 1.57 ± 0.28 1.63 ± 0.21 >0.05 2.39 ± 0.30 3.97 ± 0.33 ≤0.01
pH 6.40 ± 0.04 6.12 ± 0.03 ≤0.05 5.88 ± 0.07 5.60 ± 0.04 ≤0.01
Weight, g5 68.60 ± 1.36 69.10 ± 1.47 >0.05 NA6 NA NA
1
L* = lightness, a* = redness, b* = yellowness [L*a*b* coordinates (CIE, 1976)].
2
Values represent the mean ± SEM.
3
Carcasses that passed the inspection procedure.
4
P-values from paired t-test are reported with the Bonferroni correction.
5
Weight is of P. major and Pectoralis profundus combined.

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6
NA = not available.

were also darker, redder, and bluer (i.e., lower L* and group was found to be excellent, with ρ equal to 0.98,
higher a* and b*) than controls at 24 h after slaughter. 0.87, and 0.96 for the L*, a*, and pH measurements, respec-
Cyanotic carcasses were less acidic than controls at the tively. The control group had comparable values of ρ,
time of slaughter and 24 h later. There were no weight equal to 0.98, 0.78, and 0.91 for the L*, a*, and pH measure-
differences in the P. major. Both cyanotic and control ments, respectively.
carcasses were darker, less red, and less blue at 24 h after The Se, Sp, K, and ρ2 are shown in Table 3. The test
slaughter than at the time of slaughter. Cyanotic and with the highest Se for identifying cyanotic carcasses was
control carcasses were also more acidic at 24 h after the pH6.2 test at 85.29%, and those with the highest Sp
slaughter than at the time of slaughter. were the L*39 test and the a*4 test. The a*3 test had the
Correlation coefficients among color and pH of cyanotic best combination of Se and Sp and, hence, the highest
meat at the time of slaughter, and 24 h postmortem, are coefficient of reliability K (ρ2 = 78.93%). The pH6.3 test
shown in Table 2. The pH of meat from cyanotic carcasses also had a good coefficient of reliability K (ρ2 = 69.15%).
at slaughter time was positively and highly correlated The pH6.3 and a*3 tests had the highest agreement beyond
with the pH 24 h later. The pH was negatively and moder- chance (κ) among the tests under evaluation (κ = 0.73).
ately correlated with meat lightness at the time of slaugh-
ter and at 24 h postmortem. The pH at the time of slaugh- DISCUSSION
ter was poorly correlated with meat redness at the time
of slaughter and 24 h later. It was also negatively and Chickens were condemned for cyanosis in Canada be-
modestly correlated with the blueness of meat at the time cause the pathogenesis of the abnormal carcass color was
of slaughter and 24 h later. Color values (L*, a* and b*) hitherto unknown. This study showed that the dark color-
at slaughter time were positively and highly correlated ing of affected carcasses is compatible with a DFD-like
with their respective measurements 24 h later. condition: information that warrants review of the con-
The repeatability of pH, L*, and a* measurements demnation policy. The DFD-compatible traits included
across the four sites of the same breast of the cyanosis pH and color characteristics at the time of slaughter and
24 h postmortem. Cyanotic carcasses had a higher pH
and a correspondingly darker and redder color than con-
TABLE 2. Pearson correlations between pH and color parameters trols, and these characteristics persisted 24 h after slaugh-
from cyanotic carcasses1
ter. Thus, carcasses examined in this study showed DFD-
Pearson correlation (ρ) traits similar to those reported in other species, including
Parameters2 (n = 34)

pH0–pH24 0.64a TABLE 3. Sensitivity (Se), specificity (Sp), and coefficient of


L*0–L*24 0.43a reliability (ρ2) of tests used to identify cyanotic roasters (n = 68)
a*0–a*24 0.58a
b*0–b*24 0.58a Test cutoff1 Se Sp ρ2
pH0–L*0 −0.36a
pH0–L*24 −0.50a (%)
pH0–a*0 0.04 pH6.2 85.29 52.94 42.7
pH0–a*24 −0.1 pH6.3 76.48 91.18 69.15
pH0–b*0 −0.27 L*39 52.94 100 59.00
pH0–b*24 −0.35a L*40 61.77 91.18 54.65
a
Pearson correlations are significantly different from zero (P ≤ 0.05). L*41 67.65 76.47 44.46
1 a*3 79.41 97.06 78.93
All cases that occurred were kept in the study, hence no sampling a*4 52.94 100 59.00
scheme for cases was adopted.
2
L* = lightness, a* = redness, b* = blueness, L*a*b* coordinates (CIE, 1
L* = lightness, a* = redness, L*a*b* coordinates (CIE, 1976), based
1976). The subscripts 0 and 24 denote 0 h and 24 h, respectively. on 34 cyanotic and 34 carcasses that passed inspection.
CYANOSIS IN ROASTER BREAST MEAT 911
turkeys (Mallia et al., 1996; McCurdy et al., 1996; Barbut, recommended as a cut-off point for a pH-based test for
1998), and also to dark chickens that passed the USDA DFD (cyanosis), as indicated by the highest coefficient of
inspection (Walker and Fletcher, 1993). reliability that was observed at this pH (Table 3). In a
The identification of DFD in roaster chickens with cya- similar manner, the suggested cut-off point for L* would
nosis has important implications to the industry. One be 39 to 40, as shown by the high coefficients of reliability.
implication is that policies regarding the final disposition The a* test at a cut-off point of 3 to 4 CIE a* units was
of affected birds can be reassessed in the light of new the best overall test for the identification of cyanotic roast-
information, perhaps with these carcasses being deemed ers. In this manner, the presence of cyanosis in a carcass
suitable for human consumption. Such reassessment can be objectively determined by a color or pH measure-
would be beneficial because a substantial number (ap- ment. For example, Bisaillon et al. (1988) suggested that
proximately 0.5 million) chickens are condemned for this a visual inspection of test lacks accuracy due to the subjec-
condition annually in Canada. Recognition that DFD ex- tive interpretation of color. The availability of objective
ists in cyanotic chicken carcasses may also provide some tests could be useful to overcome these limitations. It is
insights into its eventual control by the industry. hoped that tests based on a* and pH, particularly at the

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These findings must, however, be reconciled with re- cut-off points showing high coefficient of reliability (Table
sults of several other studies that examined the relation- 3), could satisfy this need. The tests are rapid and nonde-
ship between color and pH and did not support the pres- structive and can be used on line or off line in a similar
ence of a DFD-like condition in poultry. It is noteworthy manner used for the trimming of carcasses. The use of
that none of these studies examined carcasses condemned tests in parallel did not result in an increase in the coeffi-
for cyanosis. No association between color and pH was cient of reliability. If current Canadian regulations are
found for chicken meat that passed inspection when mea- altered to allow the consumption of cyanotic birds, these
sured 24 h after slaughter (Wyers et al., 1992), and darker tests can be used to identify DFD carcasses for further
breast muscle from broiler chickens did not have a higher processing, instead of their condemnation.
pH than normal breast meat (Froning et al., 1978). Para- In summary, this study demonstrated the presence of
doxically, two separate studies found a relationship oppo- a negative correlation between lightness and pH and a
site to that observed in DFD meat, namely that redder positive correlation between redness and pH, which is
chicken meat had a correspondingly lower pH (Papinaho important for supporting the notion that meat color ob-
et al., 1996). Similarly, Boulianne and King (1995) found served in carcasses condemned for cyanosis is due to
that darker chicken meat had a correspondingly lower the presence of DFD-like traits. Cases and controls were
pH. In the present study, the pH and lightness of meat collected in a pairwise manner, and the use of a within-
from carcasses that passed inspection, at slaughter time, pair difference, as the basic test statistic, was utilized to
were not significantly correlated, which is similar to the account for similarities between a matched case and its
results of Papinaho et al. (1996). control (Martin et al., 1987). Potential confounding by
Aging cyanotic meat for 24 h under refrigeration did unmeasured factors such as climatic conditions, shipping
not result in changing darkness or redness, and differ- time, and time on the truck were accounted for in this
ences between cyanotic meat and meat that passed inspec- manner. As cases and control carcasses were also concur-
tion were still discernable, although somewhat reduced rently matched for time on the line, the pH and color
in magnitude. This result is similar to that observed in measurements should exclude time lag variation between
DFD meat in other species, in which the dark meat color slaughter and measuring the different parameters. The
persisted even when ultimate pH values were reached. DFD traits identified in this study suggest that cyanotic
Actually, several major studies on DFD pork have de- chickens, currently being condemned by AAFC, may
scribed the DFD condition at 24 h postmortem (Niel- have favorable properties for further processing such as
sen, 1981). high water-holding capacity. This study showed that tests
It has also been suggested that the darker coloring of based on spectrocolorimetry and pH show promise for
chickens condemned as cyanotic is due to an increase in detection of affected carcasses under normal plant condi-
total pigment and myoglobin content of skeletal muscle tions. However, before cyanotic carcasses can be deemed
under conditions of chronic hypoxia (Boulianne et al., safe for human consumption, the microbiological profile
1993). However, Sackett et al. (1986) showed that low and physical properties must be assessed.
partial oxygen pressure did not alter total pigment, myo-
globin, and hemoglobin concentrations in broiler muscle. ACKNOWLEDGMENTS
Hence, the role of chronic hypoxia in the occurrence of
The authors wish to acknowledge the Ontario Ministry
dark chicken carcasses remains ambiguous. In this study,
of Agriculture, Food, and Rural Affairs (OMAFRA) for
total pigment or myoglobin was not measured, and pH
their support. J. Mallia held a scholarship from the Cana-
data were consistent with DFD. Overall, one should not
dian Commonwealth Scholarship Program.
expect to observe higher pH in affected carcasses com-
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