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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 chickens condemned for cyanosis was conducted. Color (CIE L*a*b*) and pH were measured at slaughter, and after 24 h aging on ice, at four predetermined sites of the Pectoralis major. Cyanotic carcasses (dark) had a higher pH than controls at the time of slaughter and at 24 h postmortem (P < 0.01). Perimortem pH was signifi- cantly correlated with pH at 24 h postmortem (r = 0.64) and also was correlated with lightness (L*) perimortem and postmortem (24 h; r = −0.36 and 0.50, respectively). Perimortem pH was not correlated with meat redness

(a*) at slaughter time and after 24 h. Ultimate pH and lightness at 24 h postmortem were also correlated. Tests based on pH, L*, and a* of the P. major were assessed:

the sensitivity and specificity at various cut-off points 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 repeatability ( ρ ) of pH and color measurements was ex- cellent and ranged from 0.87 to 0.98. Breast meat from roasters condemned for cyanosis had dark, firm, and dry (DFD)-like traits, and accurate tests based on color and pH could be described as a means of identifying chickens condemned for cyanosis.

(Key words: broiler, dark firm dry, cyanosis, poultry color, texture)


Cyanosis is a category of condemnation adopted by Agriculture and Agrifood Canada (AAFC) to describe poultry with a dark-colored carcass and no other condem- nable lesions. Cyanosis was the fourth leading cause of condemnation of chickens in Canada in 1993 and 1994, representing almost 10% of all condemned chickens (Her- enda and Franco, 1996); roughly one million chickens were condemned for cyanosis in this period. Therefore, there is a strong interest to fully assess the situation and to examine the suitability of cyanotic carcasses for fur- ther processing. Cyanotic meat is currently condemned because little is known about its safety and quality. It has been suggested that environmental conditions producing chronic hyp- oxia, such as those observed in overcrowded poultry crates, favor the occurrence of cyanosis (Herenda and Franco, 1996). This cause has neither been confirmed nor disproved by research, as contradictory evidence has been obtained (Sackett et al., 1986; Boulianne et al., 1993). How-

Received for publication February 19, 1999.

Accepted for publication February 23, 2000.

1 To







2000 Poultry Science 79:908–912

ever, the dark coloring of cyanotic birds was suggested to be a problem related to shipping stress (Mallia, 1998). Shipment and other stressors occurring prior to slaugh- ter are believed to be responsible for the occurrence of dark, firm, and dry (DFD) conditions in other species (Tarrant, 1989; Swatland, 1994; Apple et al., 1995; Nielsen, 1981). The DFD meat has a higher pH, as has been shown in swine (Bendall and Swatland, 1988) and cattle (Tarrant, 1989). A DFD-like condition has also been observed in ducks (Chen et al., 1991) and turkeys (Mallia et al., 1996). The presence of DFD meat in other poultry appears some- what contradictory. Walker and Fletcher (1993) indicated that meat from chickens subjected to stressors was darker and had a higher pH than meat from unstressed birds, suggesting a stress-related DFD-like condition. In con- trast, the results of several other studies that examined the relationship between meat color and pH do not sup- port the presence of a DFD-like condition in inspected poultry meat (Froning et al., 1978; Wyers et al., 1992; Boulianne and King, 1995; Papinaho et al., 1996). Concerns have been expressed over the lack of stan- dardization of condemnation criteria for cyanosis in chickens. Poor diagnostic agreement for chickens con-

Abbreviation Key: AAFC = Agriculture and Agrifood Canada; DFD = dark, firm, dry; PSE = pale, soft, exudative; SE = sensitivity; SP = speci- ficity.


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mysium was left intact. Color measurements on each site were performed within 15 s of the skin removal. Chroma- ticity was measured using the color coordinates of the Commission Internationale de lEclairage (CIE, 1976) for L* (lightness), a* (redness), and b* (yellowness), under the CIE illuminant C lighting condition. After initial mea- surements, the P. major was excised, weighed, and stored on ice at 4 C for 24 h. Color measurements were then repeated in an identical fashion.

demned for cyanosis was reported in a previous study examining different condemnable conditions (Bisaillon et al., 1988), suggesting that the postmortem visual examina- tion at the abattoir may be decient in some respects. Other tests may, therefore, be of practical use to the indus- try if they improve the identication of cyanotic carcasses. For example, it may be possible to use colorimetry to objectively measure color and thereby identify cyanotic carcasses, as this method is already used to detect other commercially important meat conditions such as pale, soft, exudative (PSE) and DFD meat in pork and beef (Swatland, 1989). The main objectives of this study were 1) to investigate the presence of a DFD-like condition in roaster chickens condemned at slaughter as cyanotic,and 2) to evaluate the ability of pH and colorimetric tests to differentiate cyanotic carcasses from those that passed inspection.

MATERIALS AND METHODS Study Design and Sample Size

Sixty-eight 8-wk-old male chickens (roasters) submit-

ted to a single abattoir in southern Ontario over a 3-wk period were evaluated in a case-control study conducted in November 1996. Conventional electrical stunning and

a hot water subscald (soft scald) were used. A case (n =

34) was dened as a roaster carcass condemned by the veterinary inspector for cyanosis, and a control (n = 34) was the next fth carcass that passed the inspection proce- dure. All carcasses condemned for cyanosis during a rou- tine inspection were independently examined by the se- nior author (a veterinarian) to ensure correct classication prior to inclusion in the study. The examination consisted of a necropsy that evaluated the general appearance of the carcass, the coelom, and viscera for grossly evident pathological lesions. The roasters were raised on various farms in Southern Ontario and were of similar age, sex, and general characteristics to those raised across Ontario.

Muscle Color

The color of four specic sites of the ventral aspect of the right Pectoralis major was measured 2 within 20 min of slaughter without the removal of the overlying skin, as occurs visually during commercial inspection. The skin was patted dry with a paper towel prior to color evalua- tion. The specic sites chosen included 1) the proximal

extremity of the muscle, 2) the distal extremity of the muscle, 3) the medial side at the half-way point between the proximal and distal extremities, and 4) the lateral side at the half-way point between the proximal and distal extremities. Later, the skin overlying the breast muscle was removed, and the intact muscle was patted dry with

a paper towel prior to color evaluation; the muscle peri-

2 Chroma Meter CR-200b, Minolta, Osaka 541, Japan. 3 pH Stickmeter, Fisher Scientic, Nepean, ON, Canada, K2E 7L6.

Muscle pH

A probe 3 was used to measure the pH of the P. major

at the same four sites utilized for the color assessment. After adjusting for muscle temperature, the pH was re- corded (at a depth of 1 cm) when a stable reading was observed for 10 s. The same four muscle sites were used for ultimate pH measurements, after storage on ice for 24 h.

Statistical Analyses

A McNemars t-test was used to assess the difference

among means of the two groups as the data were paired. Four simultaneous parameters were assessed (pH, L*, a*, b*) on the same sample of each carcass. To keep the Type I error level to 5%, the Bonferroni approach to control the overall level of signicance was used (Shoukri and Edge, 1996). Pearsons correlation coefcients were used to assess linear correlations between pH and L*, a*, or b* (Snedecor and Cochran, 1980). The intraclass correlation coefcient for color and pH was based on four different sites of the P. major and was performed to assess the repeatability of color (L*, a*, b*) and pH. The ANOVA estimator of the intraclass correlation coefcient (ρ) was calculated using the one-way random effects model (Fleiss, 1986), and the time-lag was accounted for by the use of a correction factor suggested by Stanish and Tay- lor (1983). The sensitivities (Se) and specicities (Sp) of the pH, L*, and a* tests were established for the identication of cyanotic carcasses, at different cut-off points. Sensitivity was dened as the probability that a truly positive sample will test positive, and Sp was dened as the probability that a truly negative sample will test negative (Martin et al., 1987). The coefcient of reliability K ( ρ 2 ) of the pH, L*, and a* tests was also assessed (Tenenbein, 1970). Agreement among the pH test, L* test, and a* test was measured by the use of Cohens kappa statistic, κ (Cohen, 1960), divided into categories as dened by Landis and Koch (1977). This test measures the degree of agreement beyond chance.


The color and pH differences between cases and con- trols at time of slaughter and 24 h postmortem are shown in Table 1. Cyanotic carcasses were signicantly darker and redder than controls at the time of slaughter; they

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TABLE 1. Pectoralis major characteristics of roasters condemned for cyanosis and control

0.5 h

24 h

Parameter 1

Cyanosis (n = 34)

Control 2,3 (n = 34)

P-value 4

Cyanosis 2 (n = 34)

Control 2,3 (n = 34)

P-value 4

L* a* b* pH Weight, g 5

38.36 ± 0.33 4.72 ± 0.16 1.57 ± 0.28 6.40 ± 0.04 68.60 ± 1.36

41.66 ± 0.33 2.48 ± 0.14 1.63 ± 0.21 6.12 ± 0.03 69.10 ± 1.47


41.87 ± 0.55 4.51 ± 0.20 2.39 ± 0.30 5.88 ± 0.07 NA 6

47.49 ± 0.34 2.21 ± 0.13 3.97 ± 0.33 5.60 ± 0.04 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. 6 NA = not available.

were also darker, redder, and bluer (i.e., lower L* and higher a* and b*) than controls at 24 h after slaughter. Cyanotic carcasses were less acidic than controls at the time of slaughter and 24 h later. There were no weight differences in the P. major. Both cyanotic and control carcasses were darker, less red, and less blue at 24 h after slaughter than at the time of slaughter. Cyanotic and control carcasses were also more acidic at 24 h after slaughter than at the time of slaughter. Correlation coefcients among color and pH of cyanotic meat at the time of slaughter, and 24 h postmortem, are shown in Table 2. The pH of meat from cyanotic carcasses at slaughter time was positively and highly correlated with the pH 24 h later. The pH was negatively and moder- ately correlated with meat lightness at the time of slaugh- ter and at 24 h postmortem. The pH at the time of slaugh- ter was poorly correlated with meat redness at the time of slaughter and 24 h later. It was also negatively and modestly correlated with the blueness of meat at the time of slaughter and 24 h later. Color values (L*, a* and b*) at slaughter time were positively and highly correlated with their respective measurements 24 h later. The repeatability of pH, L*, and a* measurements across the four sites of the same breast of the cyanosis

TABLE 2. Pearson correlations between pH and color parameters from cyanotic carcasses 1

Parameters 2

Pearson correlation (ρ) (n = 34)

pH 0 pH 24 L* 0 L* 24 a* 0 a* 24 b* 0 b* 24 pH 0 L* pH 0 L* pH 0 a* pH 0 a* pH 0 b* pH 0 b*
























a Pearson correlations are signicantly different from zero (P 0.05). 1 All cases that occurred were kept in the study, hence no sampling scheme for cases was adopted. 2 L* = lightness, a* = redness, b* = blueness, L*a*b* coordinates (CIE, 1976). The subscripts 0 and 24 denote 0 h and 24 h, respectively.

group was found to be excellent, with ρ equal to 0.98, 0.87, and 0.96 for the L*, a*, and pH measurements, respec- tively. The control group had comparable values of ρ, equal to 0.98, 0.78, and 0.91 for the L*, a*, and pH measure- ments, respectively. The Se, Sp, K, and ρ 2 are shown in Table 3. The test with the highest Se for identifying cyanotic carcasses was the pH 6.2 test at 85.29%, and those with the highest Sp were the L* 39 test and the a* 4 test. The a* 3 test had the best combination of Se and Sp and, hence, the highest coefcient of reliability K ( ρ 2 = 78.93%). The pH 6.3 test also had a good coefcient of reliability K ( ρ 2 = 69.15%). The pH 6.3 and a* 3 tests had the highest agreement beyond chance (κ) among the tests under evaluation ( κ = 0.73).


Chickens were condemned for cyanosis in Canada be- cause the pathogenesis of the abnormal carcass color was hitherto unknown. This study showed that the dark color- ing of affected carcasses is compatible with a DFD-like condition: information that warrants review of the con- demnation policy. The DFD-compatible traits included 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- trols, and these characteristics persisted 24 h after slaugh- ter. Thus, carcasses examined in this study showed DFD- traits similar to those reported in other species, including

TABLE 3. Sensitivity (Se), specificity (Sp), and coefficient of reliability (ρ 2 ) of tests used to identify cyanotic roasters (n = 68)

Test cutoff 1



ρ 2






































1 L* = lightness, a* = redness, L*a*b* coordinates (CIE, 1976), based on 34 cyanotic and 34 carcasses that passed inspection.

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recommended as a cut-off point for a pH-based test for DFD (cyanosis), as indicated by the highest coefcient of reliability that was observed at this pH (Table 3). In a similar manner, the suggested cut-off point for L* would be 39 to 40, as shown by the high coefcients of reliability. The a* test at a cut-off point of 3 to 4 CIE a* units was

the best overall test for the identication of cyanotic roast- ers. In this manner, the presence of cyanosis in a carcass can be objectively determined by a color or pH measure- ment. For example, Bisaillon et al. (1988) suggested that

a visual inspection of test lacks accuracy due to the subjec-

tive interpretation of color. The availability of objective tests could be useful to overcome these limitations. It is hoped that tests based on a* and pH, particularly at the cut-off points showing high coefcient of reliability (Table 3), could satisfy this need. The tests are rapid and nonde- structive and can be used on line or off line in a similar manner used for the trimming of carcasses. The use of tests in parallel did not result in an increase in the coef- cient of reliability. If current Canadian regulations are altered to allow the consumption of cyanotic birds, these tests can be used to identify DFD carcasses for further processing, instead of their condemnation. In summary, this study demonstrated the presence of

a negative correlation between lightness and pH and a positive correlation between redness and pH, which is important for supporting the notion that meat color ob- served in carcasses condemned for cyanosis is due to the presence of DFD-like traits. Cases and controls were collected in a pairwise manner, and the use of a within- pair difference, as the basic test statistic, was utilized to account for similarities between a matched case and its control (Martin et al., 1987). Potential confounding by unmeasured factors such as climatic conditions, shipping time, and time on the truck were accounted for in this manner. As cases and control carcasses were also concur- rently matched for time on the line, the pH and color measurements should exclude time lag variation between slaughter and measuring the different parameters. The DFD traits identied in this study suggest that cyanotic chickens, currently being condemned by AAFC, may have favorable properties for further processing such as high water-holding capacity. This study showed that tests based on spectrocolorimetry and pH show promise for detection of affected carcasses under normal plant condi- tions. However, before cyanotic carcasses can be deemed safe for human consumption, the microbiological prole and physical properties must be assessed.

turkeys (Mallia et al., 1996; McCurdy et al., 1996; Barbut, 1998), and also to dark chickens that passed the USDA inspection (Walker and Fletcher, 1993). The identication of DFD in roaster chickens with cya- nosis has important implications to the industry. One implication is that policies regarding the nal disposition of affected birds can be reassessed in the light of new information, perhaps with these carcasses being deemed suitable for human consumption. Such reassessment would be benecial because a substantial number (ap- proximately 0.5 million) chickens are condemned for this condition annually in Canada. Recognition that DFD ex- ists in cyanotic chicken carcasses may also provide some insights into its eventual control by the industry. These ndings must, however, be reconciled with re- sults of several other studies that examined the relation- ship between color and pH and did not support the pres- ence of a DFD-like condition in poultry. It is noteworthy that none of these studies examined carcasses condemned for cyanosis. No association between color and pH was found for chicken meat that passed inspection when mea- sured 24 h after slaughter (Wyers et al., 1992), and darker breast muscle from broiler chickens did not have a higher pH than normal breast meat (Froning et al., 1978). Para- doxically, two separate studies found a relationship oppo- site to that observed in DFD meat, namely that redder chicken meat had a correspondingly lower pH (Papinaho et al., 1996). Similarly, Boulianne and King (1995) found that darker chicken meat had a correspondingly lower pH. In the present study, the pH and lightness of meat from carcasses that passed inspection, at slaughter time, were not signicantly correlated, which is similar to the results of Papinaho et al. (1996). Aging cyanotic meat for 24 h under refrigeration did not result in changing darkness or redness, and differ- ences between cyanotic meat and meat that passed inspec- tion were still discernable, although somewhat reduced in magnitude. This result is similar to that observed in DFD meat in other species, in which the dark meat color persisted even when ultimate pH values were reached. Actually, several major studies on DFD pork have de- scribed the DFD condition at 24 h postmortem (Niel- sen, 1981). It has also been suggested that the darker coloring of chickens condemned as cyanotic is due to an increase in total pigment and myoglobin content of skeletal muscle under conditions of chronic hypoxia (Boulianne et al., 1993). However, Sackett et al. (1986) showed that low partial oxygen pressure did not alter total pigment, myo- globin, and hemoglobin concentrations in broiler muscle. Hence, the role of chronic hypoxia in the occurrence of dark chicken carcasses remains ambiguous. In this study, total pigment or myoglobin was not measured, and pH data were consistent with DFD. Overall, one should not expect to observe higher pH in affected carcasses com- pared with controls if the color change was simply due to increased pigment level. To assist processors, cut-off points for pH, L*, and a* tests were examined. In general, a pH of 6.3 could be


The authors wish to acknowledge the Ontario Ministry of Agriculture, Food, and Rural Affairs (OMAFRA) for their support. J. Mallia held a scholarship from the Cana- dian Commonwealth Scholarship Program.


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