Current state of breast meat quality in standard-yielding broiler strains

On d 14 and 33, a total of 24 birds (n = 6 per strain and sex) were randomly selected and euthanized by cervical dislocation, and a sample of 3 to 5 g of muscle tissue was taken from the ventral (skin) surface of the cranial (the thickest) part of the P. major muscle for in vitro modeling of postmortem pH changes of this muscle (Figure 1). The samples were transported to the laboratory (Department of Animal Science, Université Laval, Quebec, Canada) on dry ice and kept at −80°C until analysis. To measure changes in postmortem muscle pH between strains and sexes and with age, the in vitro model described in Baldi et al. (2020) was used. For this, frozen muscle tissues sampled shortly (<5 min) after death were powdered in liquid nitrogen, homogenized at 1:10 (weight/volume) ratio in glycolysis buffer (5 mM MgCl₂, 10 mM Na₂HPO₄, 60 mM KCl, 5 mM Na-ATP, 0.5 mM ADP, 0.5 mM NAD⁺, 25 mM carnosine, 30 mM creatine, 40 mM glycogen, and 10 mM sodium acetate) at pH 7.4. Reaction tubes were incubated in a water bath at 25°C for the duration of the analysis. At time 0, 15, 30, 60 (1 h), 120 (2 h), 180 (3 h), 240 (4 h), 360 (6 h), and 1,440 (24 h) min postincubation, the pH was measured using a portable pH-meter (Ross, Orion Star A221, Thermo Scientific, Beverly, CA) combined with an Orion Kniphe electrode (ThermoFisher, Nepean, ON, Canada). First, a 0.5 mL of the incubated preparation was transferred into 2 mL tube and homogenized with 1.5 mL of a buffer containing 25 mM of sodium iodoacetate and 750 mM of KCl solution (pH 7.0). The pH was measured by direct insertion of the electrode of the pH-meter into the 2 mL tube after centrifugation at 17,000× g for 5 min and temperature equilibration at 25°C. Samples were analyzed in duplicates for all pH measurements.

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Figure 1. Breast muscle samples for in vitro glycolysis analysis were taken from the cranial part of the ventral (skin) side of the Pectoralis major muscle indicated by the rectangle.

The effect of the strain-by-sex interaction on BW5, carcass, and carcass cuts yield was not significant (Table 1). On d 35, processed broilers from the Cobb 500 strain had a significantly higher BW (+176 g), greater BMY (+1.21 percentage points), and higher yield of the P. major muscle (+1.07 percentage points) when compared with the Ross 308 strain. However, broilers from the Ross 308 strain had a significantly higher thigh yield (+1.17 percentage points) and slightly but significantly greater yield of the upper part of the thigh (+0.82 percentage points) and drumsticks (+0.30 percentage points). The differences in BW5 and meat yield could be only partly explained by differences in feed intake as this trait only tended to be influenced by the strain effect (P = 0.055) at the end of the experiment (3,751.0 ± 53.7 and 3,589.0 ± 53.7 kg of feed /bird for Cobb 500 and Ross 308, respectively). However, these findings agree with previous studies reporting that variability in BW and in the yield of carcass cuts was also explained by differences in the genetic background of the birds (Acar et al., 1991; Brewer et al., 2012; Trocino et al., 2015; Santos et al., 2021). Under our experimental conditions, broilers from the Cobb 500 strain exhibited greater yield of upper body cuts (whole breast and P. major), whereas broilers from the Ross 308 strain exhibited higher yield of lower body cuts (thigh, upper thigh, and drumsticks). In a previous study, researchers compared broilers from the Ross 308 strain with broilers from the Ross 708 strains and showed that the Ross 308 strain was characterized by a higher leg meat yield (Da Costa et al., 2017).

Based on the 95% CI, allometric growth coefficients were not significantly different between strains or sexes (Table 2). These findings were not unexpected because the shape of the growth curve of carcass cuts is largely influenced by genetics and genetic selection (Zuidhof et al., 2014), and both Cobb 500 and Ross 308 are selected for similar criteria (i.e., growth rate and BMY). Interestingly, the allometric coefficient for the whole breast and that of the P. major muscle in both sexes of the Cobb 500 strain were significantly higher than unity, which was not the case for the Ross 308 strain. This indicates that relative to the whole carcass, both the whole breast and the P. major muscle were growing at a faster rate than other cuts in the Cobb 500 stain, which could have contributed to the higher BMY of this strain. However, the overlapping confidence intervals of the allometric coefficients of the whole breast and of the P. major muscle between the 2 strains suggests that the faster growth of these 2 cuts in the Cobb 500 strain was not enough to induce a significant shift in the shape of the growth curve of these cuts when compared with the Ross 308 strain. Finally, of all growth coefficients, the only ones that were significantly lower than unity were these of the wings in male Cobb 500 and female Ross 308, but their confidence intervals were overlapping, indicating that the wings grew at a slower rate than the rest of the carcass and that this growth rate was similar in both strains. Overall, our findings suggest that both strains and sexes have similar growth curves of carcass cuts, and that these cuts grow at a similar rate.

White striping is characterized by the presence of white striations on the skin side of the P. major muscle, running in parallel to the direction of muscle fibers and having variable thickness according to their severity scores (Kuttappan et al., 2012). In the current study, very few fillets exhibited only WS (1.87% of 160 evaluated fillets), and most WS cases were observed on fillets that were also WB-affected (15.62% of 160 evaluated fillets: 8.12% in Cobb 500 and 7.5% in Ross 308). The co-occurrence of these 2 myopathies has already been reported in the literature (Mudalal et al., 2015; Soglia et al., 2016), with one possible explanation being that WS could progress and lead to the development of WB (Griffin et al., 2018). In our analysis, we considered WS independently from WB and found that neither strain nor sex had a statistically significant effect on the score of this myopathy (Table 3). In the current study, almost all WS cases were mild and occurred at a similar frequency in both strains (8.12% and 8.75% in Cobb 500 and Ross 308, respectively) and sexes (9.37% and 7.50% in males and females, respectively), which is probably the reason for the lack of significant differences reported above.

Wooden breast is characterized by increased hardness of the P. major muscle that is focal and localized to the cranial part of the muscle in mild to moderate forms, or is diffused to the caudal part leading to a pronounced hardness of the entire muscle accompanied with hemorrhages (petechiae) and the accumulation of a viscous exudate on the surface of the muscle in the severe forms (Sihvo et al., 2014; Tijare et al., 2016; Griffin et al., 2018). In the present study, mild and moderate WB accounted for most cases of WB observed on the 160 evaluated breast fillets (normal: 21.25% vs. 18.75%, mild: 22.5% vs. 15.62%, moderate: 4.38% vs. 12.5% and severe: 1.88% vs. 3.12% for Ross 308 and Cobb 500, respectively). A Chi-squared analysis revealed that the 2 strains only significantly differed in the moderate category of WB with breast fillets from the Cobb 500 strain being 2.8 times (P = 0.01) more represented in this category than breast fillets of the Ross 308 strain. A similar analysis showed that breast fillets from male Cobb 500 broilers accounted for the majority of breast fillets exhibiting moderate WB (10%, 2.5%, 2.5% and 1.88% for male and female Cobb 500 birds and for male and female Ross 308 birds, respectively). Further analysis revealed a significant effect of strain and sex on the average score of WB (Table 3), and the interaction between these 2 factors tended to be statistically significant with females of both strains exhibiting similar WB average scores and Cobb 500 males exhibiting higher score than their Ross 308 counterparts (Figure 2) which in line with the above-reported frequencies. The development of WB is associated with increased breast muscle development (Petracci et al., 2015; Trocino et al., 2015; Sihvo et al., 2017; Griffin et al., 2018; Pampouille et al., 2019). As shown in Tables 1 and 2, birds from the Cobb 500 strain had a significantly higher yield of the P. major muscle than birds from the Ross 308 strain, and also had an allometric growth coefficient significantly greater than unity, reflecting higher growth of this muscle relative to the rest of the carcass. Consequently, Cobb 500 birds were more susceptible to the development of WB and had a significantly higher WB score. To further illustrate the relationship between strain, muscle growth, and WB, we analyzed the yield of the P. major muscle and that of BMY as a function of the interaction between the strain and WB category while accounting for the effect of sex. The effect of the strain-by-WB interaction was statistically significant (P < 0.001 for both P. major yield and BMY). As can be seen on Figures 3A and 3B, increased muscle yield was associated with increased severity of WB in the Cobb 500 strain, with a similar but less clear trend in the Ross 308 strain because of the lower frequency of severe WB. Moreover, we found a similar relationship between BW at slaughter and WB (P < 0.001, Figure 3C), and between carcass weight and WB (P < 0.001, Figure 3D). Therefore, our data are in agreement with the above-cited literature showing that the occurrence and severity of WB are determined by body and carcass weight, muscle growth, and BMY. The role of increased growth and muscle development in the development of WB was also supported by the results of the binomial regression model that was fitted to the severity scores after recoding them into a binary trait with the score of zero representing normal fillets while scores greater than zero represented WB-affected fillets. According to this model, the effect of strain per se on the occurrence of WB was not significant (P = 0.22). However, the effect of BW (OR = 1.001, 95% CI = 1.0007–1.002, P < 0.001) and of BMY (OR = 1.51, 95% CI = 1.22–1.87, P < 0.0001) on the occurrence of this myopathy was highly significant. Based on these results, BMY was the principal driver of the occurrence of WB with a 1 unit increase in BMY being associated with a 51% increase in the odds of breast fillets developing some degree of WB. The logistic regression model was then used to predict the probability of breast fillets switching from normal to WB-affected in the range of BMY observed in the present study (Figure 4). The findings from this analysis emphasized the key role of increased muscle growth in the development of WB.

Breast Meat Quality Traits

The ultimate pH of the P. major muscle (PM-pHu) is a major determinant of the technological quality traits of broiler breast meat and is largely determined by genetics (Le Bihan-Duval et al., 2008; Alnahhas et al., 2014). Normal breast meat is characterized by an average pHu of 5.7 to 5.9. Values higher than 6.1 or lower than 5.7 are associated with development of meat quality defects including DFD and acid meat, respectively (Zhang and Barbut, 2005). In the present work, the P. major muscle of broilers from the Ross 308 strain exhibited a slightly but significantly higher PM-pHu than the Cobb 500 strain (+0.03 pH units). In contrast, the effect of sex on PM-pHu was not significant (Table 4). These findings are in line with a previous study that compared the PM-pH of males and females from 4 different strains between 2 and 24 h postmortem, and reported no differences between sexes at all measurement times (Brewer et al., 2012). Interestingly, the effect of the strain-by-sex interaction on PM-pHu tended to be statistically significant (P = 0.06). As can be seen in Figure 5, females from the Cobb 500 strain had a lower PM-pHu than females from the Ross 308 strain, while males from both strains had a similar PM-pHu. Usually, WB-affected breast fillets exhibit higher PM-pHu than normal fillets (Baldi et al., 2020). In the current study, the presence of WB had no effect on PM-pHu, probably because only few severe cases of WB were found in the population of samples. Finally, the PM-pHu values reported in the current study were within the normal range of 5.7 to 5.9 reported previously (Brewer et al., 2012; Alnahhas et al., 2014; Maynard et al., 2023).

Table 4. Effect of strain, sex, and their interaction on breast meat quality traits.¹

Empty Cell	Strain		Sex		P-value
Trait2	Ross 308	Cobb 500	Male	Female	Strain	Sex	I3
PM-pHu	5.84 ± 0.01a	5.81 ± 0.01b	5.82 ± 0.01	5.82 ± 0.01	0.03	0.77	0.06
L*	56.19 ± 0.36	56.94 ± 0.36	56.51 ± 0.36	56.63 ± 0.36	0.14	0.81	0.34
a*	6.58 ± 0.32	7.02 ± 0.32	7.41 ± 0.32a	6.18 ± 0.32b	0.34	0.008	0.51
b*	17.21 ± 0.31	17.91 ± 0.31	17.28 ± 0.31	17.84 ± 0.31	0.11	0.21	0.31
Drip loss, %	3.08 ± 0.20b	3.96 ± 0.20a	3.32 ± 0.20	3.72 ± 0.20	0.01	0.19	0.32
Cooking loss, %	17.90 ± 0.33b	19.32 ± 0.33a	19.47 ± 0.33a	17.76 ± 0.33b	0.01	0.004	0.49
WBSF, N/cm2	25.75 ± 1.08	26.26 ± 1.08	25.89 ± 1.08	26.12 ± 1.08	0.56	0.79	0.99

1

Data are presented as least squares means and their standard errors (n = 40 birds/strain/sex).

2

PM-pHu: The ultimate pH of the Pectoralis major muscle, L*: Lightness index of the Pectoralis major muscle, a*: Redness index of the Pectoralis major muscle, b*: Yellowness index of the Pectoralis major muscle, WBSF: Warner-Bratzler shear force.

3

P-value of the strain-by-sex interaction. Means within a row lacking a common superscript differ (P < 0.05).

Figure 5. Effect of the strain-by-sex interaction on the ultimate pH of the Pectoralis major muscle. *The difference is statistically different at P < 0.05.

Color parameters of the P. major muscle were also measured in the current work, because they have an important impact on consumer acceptance of breast meat and could influence the final purchasing decision (Droval et al., 2012). Our findings did not reveal any significant differences in L*, a*, and b* between strains. Lopez et al. (2011) compared 2 commercial strains of broiler chickens and also reported no significant differences in color parameters on the bone side of the P. major muscle at 24 h postmortem. L* values were not influenced by sex, which is in agreement with findings from Brewer et al. (2012) who compared L* values of breast fillets from males and females at 24 h postmortem and found no significant differences when fillets were deboned at 2 h postmortem. However, the redness index (a*) was significantly different between sexes, with males exhibiting higher a* value than females; this also agrees with a previous study that compared standard-yielding and high-yielding strains and reported that the a* of breast fillets from different strains was higher in males than in females (Maynard et al., 2023). Breast meat color parameters can vary with extreme variations in muscle pH, leading to the development of the specific phenotypes of meat quality defects such as PSE-like and DFD meat (Allen et al., 1997; Barbut, 1997; Allen et al., 1998; Zhang and Barbut, 2005). In the current study, the small difference in PM-pHu between strains and the lack of a significant difference in PM-pHu between sexes have probably contributed to the lack of significant differences in color parameters between different groups. The between-sex difference in a* could be associated with the greater score of WB observed in males than in females, which agrees with a previous report showing that the presence of WB was associated with increased redness in myopathic breast fillets (Baldi et al., 2019).

WHC is an important technological quality trait because it not only influences meat juiciness and thus consumer experience, but it also has a major impact on meat yield after transformation. The PM-pHu is an important determinant of WHC of breast meat (Bowker and Zhuang, 2015), with lower values of PM-pHu being associated with higher DL and CL (Barbut et al., 2005; Zhang and Barbut, 2005; Alnahhas et al., 2014). Accordingly, the slight decrease in PM-pHu in Cobb 500 birds could have partly contributed to the slight but significant increase in the DL (+0.87%) and CL (+1.42%) in the breast meat of this strain compared with that of the Ross 308 strain. More importantly, breast fillets of Cobb 500 broilers exhibited a higher WB score than the Ross 308 broilers, which was previously shown to increase CL and DL (Soglia et al., 2016). In fact, we found a statistically significant strain-by-WB interaction for CL in evaluated breast fillets (P < 0.0001). As can be seen on Figure 6, increased degree of WB was associated with increased CL in Cobb 500. A similar but less clear trend was observed in breast fillets from the Ross 308 strain. Males’ breast fillets had a significantly higher CL than that of females (+1.71%), and this higher loss is in agreement with findings from the literature showing a higher CL in males than in females (Brewer et al., 2012; Maynard et al., 2023). Similar to the strain-by-WB interaction, a significant sex-by-WB interaction was found for CL in the present study (P < 0.0001). In males, CL increased significantly with increased WB degree, while in females the increase in CL was less pronounced (Figure 7).

Figure 6. Effect of the strain-by-wooden breast interaction on breast meat cooking loss. The X-axis represents the interaction between strain and the categories of the wooden breast myopathy (normal, mild, moderate and severe).

Figure 7. Effect of the sex-by-wooden breast interaction on breast meat cooking loss. Wooden breast categories are 0: normal, 1: mild, 2: moderate, and 3: severe.

The texture of cooked breast meat did not differ between strains or sexes. Just like WHC, Warner-Bratzler shear force (WBSF) is also influenced by variations in the PM-pHu (Alnahhas et al., 2014). Under lower PM-pHu values, CL is increased leading to increased WBSF and decreased meat tenderness (El Rammouz et al., 2004). In the present study, the differences in CL between strains (1.42 percentage points) and sexes (1.71 percentage points) did not seem to be pronounced enough to induce a change in WBSF. Severe cases of WB are also known to increase the hardness of breast fillets as measured by the compression test on raw meat or by a texture profiler used on cooked meat (Soglia et al., 2016). However, WB was not associated with changes in WBSF of cooked meat in the present study which can be probably attributed to the low frequency of severe degrees of WB in this study. Furthermore, the technique used to measure changes in the textural properties of breast fillets could have an impact on the results. In a recent study, WB-affected fillets obtained from carcasses that were deboned at different postmortem times and cooked at 24 h postmortem did not exhibit any changes in texture measured by the compression test, WBSF or the blunt Meullenet–Owens razor shear (Tasoniero et al., 2020). The mechanism underlying differences in hardness measurements obtained from different measurement techniques applied to WB-affected fillets require further research to be elucidated.

Based on the above findings, both strains used in the present study had only slightly different technological quality attributes of breast meat. The reported significant differences in DL and CL could not be fully explained by differences in muscle pHu and were significantly influenced by the presence of WB. Overall, the findings highlight the negative relationship between increased growth and muscle development on one hand, and meat quality on the other hand.

Postmortem Energy Metabolism

The rate and extent of the postmortem decline of muscle pH determines the quality of breast meat in broiler chickens. Faster rate of postmortem decline of muscle pH is the underlying cause of PSE-like meat in broiler chickens (Barbut, 1997; Sheard et al., 2012), while low and high PM-pHu are the underlying causes of acid and DFD meat, respectively (Alnahhas et al., 2014; Harford et al., 2014). Genetics is one of the major factors known to influence the PM-pHu (Le Bihan-Duval et al., 2008; Le Bihan-Duval et al., 2018); therefore, the effect of strain on changes in postmortem muscle pH should be investigated. According to the results from the in vitro glycolysis conducted on breast muscle samples from the investigated strains, the postmortem decline of muscle pH was significantly influenced by strain (P < 0.0001), the time of measurement (P < 0.0001), the age of the birds at sampling (P < 0.0001), and the 3-way interaction between these factors (P < 0.0001). At 14 d of age (Figure 8A), the initial pH was significantly higher in the P. major muscle of Cobb 500 broilers than in Ross 308 broilers (6.54 vs. 6.41). At 15 min postmortem, the between-strain difference was no longer significant. In addition, the values were slightly lower (6.35 and 6.24 for Cobb 500 and Ross 308, respectively) than pH values reported for male Ross 308 at 15 min in normal (> 6.5) breast meat (Baldi et al., 2020), which is probably because of the complexity of the muscle environment and the difficulty of replicating this environment in vitro. At 180 min postmortem, the pH of the P. major muscle reached its ultimate point (5.78 and 5.75 for Cobb 500 and Ross 308, respectively). In the Ross 308 strain, the pHu remained stable between 180 min and 24 h postmortem, while in the Cobb 500 strain, the pHu continued to slightly decrease, although the between-strain difference was not statistically significant at 24 h postmortem. At 33 d of age (Figure 8B), the initial pH of the P. major muscle was similar in the 2 strains (6.35 and 6.47 for Cobb 500 and Ross 308, respectively). However, the pH declined significantly faster in the Cobb 500 strain than in the Ross 308 strain between 15 and 60 min postmortem. At 120 min postmortem, the between-strain difference in muscle pH was no longer significant, and the pH reached its ultimate point at 180 min postmortem and remained stable up to 24 h postmortem.

Figure 8. Strain effect on the rate and extent of postmortem pH decline in the Pectoralis major muscle sampled at 14 (A) and 33 (B) days of age.

With regard to the sex effect, the rate and extent of decline of the pH was similar for males and females at 14 and 33 d. Moreover, the pH reached its ultimate point at 180 min postmortem and remained stable up to 24 h postmortem in both sexes (Data not shown).

The in vitro data obtained from samples taken on d 14 and d 33 from both strains suggest that the onset of rigor mortis in the P. major muscle could start as early as 3 h postmortem, when the pH attains its ultimate point of decline. In an earlier study from 2005, the onset of rigor mortis was reported to start in the P. major muscle between 4.5 and 6 h postmortem (Thielke et al., 2005). This difference would suggest that postmortem energy (i.e., ATP) production in the P. major muscle of today’s strains ceases earlier, causing the muscle to enter a state of rigor mortis earlier as the actomyosin bridges stabilize in the absence of ATP. The lower energy store in the P. major muscle in modern strains can be attributed to the continuous genetic selection to increase BMY. Posthatch breast muscle growth operates by increasing the length and the diameter of muscle fibers (Remignon et al., 1995; Velleman, 2019), and this increase in muscle fiber diameter (or muscle fiber hypertrophy) is associated with a decrease in the glycolytic potential of the muscle (Berri et al., 2001, 2007). Consequently, over generations of selection to increase BMY, the glycolytic reserves stored in the P. major muscle at the age of processing decreases, leading to earlier cessation of postmortem acidification in the P. major muscle of birds from strains available on today’s market than in birds from the same strains but from 15 or 20 years ago. In this study, we used 6 samples per strain and sex to perform the in vitro glycolysis. Future studies should use a larger sample size to validate the findings and further investigate the relationship between myofiber hypertrophy and energy metabolism.

Findings from the in vitro glycolysis model are of interest for meat quality, because deboning of breast fillets before the onset of rigor mortis (while ATP is still present in the muscle) can increase shortening of the muscle and increase its hardness (Cavitt et al., 2004, 2005). Finally, the marked decrease in muscle energy stores in the P. major muscle could impede muscle function and contribute to the development of breast muscle myopathies. In fact, multiple studies from the literature have reported a lower glycolytic potential or glycogen reserve at death coupled with altered utilization of glycolysis intermediates in WB-affected muscles (Abasht et al., 2016; Zambonelli et al., 2016; Boerboom et al., 2018; Baldi et al., 2020).

CONCLUSIONS AND APPLICATIONS

• 1.

  Birds from the Cobb 500 strain had higher body weight, greater breast meat yield, and tended to have higher total feed consumption than birds from the Ross 308 strain at 35 d.

• 2.

  Breast fillets from the Cobb 500 strains exhibited higher wooden breast score, greater drip loss, and greater cooking loss than fillets from the Ross 308 strain.

• 3.

  Breast muscles from today’s strains seem to enter rigor mortis at least 1 h earlier than previously reported in the literature.

• 4.

  Increased growth and muscle development have adverse effects on breast meat quality. Thus, the choice of strain and sex for broiler production requires finding a compromise between yield and quality.

Source: Science Direct