1. Introduction
The intensification of poultry production and genetic selection programs prioritizing fast growth and high breast yield have resulted in the emergence of growth-related myopathies in broiler chickens [
1,
2]. Spaghetti meat (SM), characterized by overall impaired muscle integrity with separation of the fibers [
3], is the latest abnormality identified, leading to degenerative disorders in broiler muscle tissues. However, SM remains inadequately understood. In contrast, white striping (WS), marked by white striations of the
pectoralis major muscle parallel to the fibers [
4], and wooden breast (WB), characterized by fibrosis and
pectoralis major hardness [
5], have been subjected to extensive investigation [
1,
6,
7]. Under commercial conditions, the occurrence of mild or moderate WS, severe WB, and SM can reach up to 96.0%, 11.8%, and 36.3%, respectively [
8]. A recent meta-analysis of experimental data reported the highest occurrence of WS myopathy (64.7%), followed by SM (12%) and WB (11%) [
9].
Severely affected meat faces consumer rejection and cannot always be marketed as fresh; it is redirected as raw material for processing or degraded to pet food [
6,
10]. Zanetti et al. [
11] evaluated that in Brazil, approximately 0.8% of chicken breasts were condemned due to WB and WS, accounting for up to USD 70,632 in daily losses. In North America, the economic impact of these myopathies in broiler chickens was estimated to exceed USD 1 billion [
12].
Defective
pectoralis major meat shows changes in its chemical composition, reflected mainly in reduced protein levels, increased moisture and fat content [
13,
14,
15], and altered fatty acid [
16,
17] and amino acid profiles [
15,
18] compared to normal breast meat. Although these changes are not severe enough to challenge the nutritional value of chicken meat—owing to their low absolute values—they can significantly impair the appearance and technological properties of the breast, such as color, texture, water holding, and binding capacity. Such impairments can dramatically limit the performance of the meat in further processed products, depending on the severity of the myopathy and the extent of structural changes [
1,
19,
20]. Thus, although growth-related myopathies do not pose a public safety risk [
17,
21], they represent substantial economic losses [
12] and a challenge to the sustainability of the broiler production chain [
22].
The impact of SM, the most recently observed myopathy, on meat quality has been investigated to a lesser extent compared to WS and WB. Only limited reports are available on alterations in the fatty acid profile [
14] and mineral composition [
23] in SM, and currently, there are no data on the amino acid composition of SM. To our knowledge, only one study simultaneously examined the effects of these three main growth-related abnormalities on meat quality traits [
14]. In addition, while Wang et al. [
24] recently reported the combined effects of these myopathies on the textural and physical quality traits of chicken fillets, no comparative data are available regarding the differences in nutritional value and sensory attributes between WS, SM, WB, and normal meat.
Therefore, the present study aimed to provide a comprehensive evaluation of the effects of growth-related myopathies on the physical, chemical, nutritional, and sensory properties of chicken breast by assessing the technological, chemical, fatty acid, mineral, and amino acid compositions, as well as protein and lipid oxidation, in comparison to the sensory properties of normal breasts and pectoralis major muscles affected by WS, WB, and SM. The associated nutritional and health indices were also calculated.
3. Results and Discussion
The rate of myopathies observed in this study was moderate for WS (25.5%) and SM (18.3%) and low for WB (8.9%). These myopathy rates differ remarkably across studies, with WS ranging from 9.8% to 89.0% [
40,
41], SM from 6.2% to 89.2% [
30,
40], and WB from 16.7% to 37.3% [
8,
42]. The relatively low occurrence of WB in our samples can be considered a limitation of this study. Nevertheless, other research has also shown unbalanced sample sets due to the low occurrence or small number of WB (
n = 5) cases [
18,
43] or normal breasts (only 4 normal breast samples out of 183 in 6-week-old broilers) [
44]. It should be noted that the occurrence of WB and other myopathies in vivo is unpredictable and can only be confirmed post-mortem. A comparison across studies is difficult since myopathy rates can depend on several factors, e.g., body weight, breast yield, growth rate, and bird age [
8,
9,
45,
46]. It is worth highlighting that mild-to-moderate WS and WB were observed in the breast meat in the present study, whereas no severe WS or WB was found.
Regarding meat quality, the effects of myopathies on breast quality traits are presented in
Table 1. Generally speaking, the presence of myopathies is known to impair meat quality by affecting its technological properties and limiting its suitability for further processing, with the extent of these effects depending on myopathy severity [
1,
19,
20]. In the present study, the pH of the meat did not differ among the groups (
p = 0.627), corroborating previous findings [
3,
47,
48]. Regarding color, the presence of myopathies did not affect L* values (
p = 0.670), as previously reported [
47,
49,
50]. Nevertheless, the presence of WB reduced the a* index compared to WS (−74.5%), SM (−73.8%), and normal breasts (−73.1%) (
p = 0.040), as well as the b* index compared to WS meat (−26.8%;
p = 0.044). In contrast, some studies found that the redness of breast meat increased in the presence of WB [
51,
52,
53,
54], which can be attributed to the bulge and pale areas of WB-affected meat. On the other hand, other studies reported no effect on a* values [
3,
9,
23,
48]. Compared to normal meat, as shown in
Table 1, WB meat had higher cooking losses (+13.7%;
p = 0.002), whereas thawing losses did not differ among the groups (
p = 0.736). The decrease in protein content (as reported in
Table 2) and muscle fiber degeneration—which usually retain water—likely contributed to changes in thawing and cooking losses of defective meat [
20]. Our findings are consistent with previous studies that identified increased cooking losses as an issue linked to WB [
1,
29,
47]. Additionally, cooked WB samples exhibited higher shear force compared to SM samples (+19.9%;
p = 0.041), with no differences between WB, SM, and normal meat. The TPA analysis (
Table 1) did not reveal any changes in hardness, springiness, cohesiveness, or chewiness between the normal and defective meat, nor among the meat affected by the different myopathies (
p > 0.05). Therefore, differences in texture according to the presence of myopathies depend on different factors. On the one hand, the increase in shear force measured in WB meat in comparison to SM is likely due to the greater cooking losses and collagen deposition in the former compared to the latter [
14]. Therefore, SM is characterized by the rarefication of connective tissue, resulting in a softer texture, as previously reported in other studies [
14,
48]. FTIR spectroscopic and histological analyses found that the texture differences between WB meat and SM could be due to the differences in collagen fiber molecular structure and connective tissue organization. Specifically, collagen in the perimysium of WB-affected muscles is more abundant and consists of both thin and thick, randomly organized collagen fibers [
55]. In contrast, SM is characterized by randomly organized, thinner, and looser immature collagen fiber bundles. In fact, Pascual et al. [
48] found that (i) more force was needed to shear WB samples compared to SM samples using an Allo–Kramer blade (Texture Technologies Corp., Hamilton, MA, USA), as indicated by a larger area under the force deformation curve; and (ii) fewer peaks were recorded for WB compared to normal meat during the Meullenet–Owens razor shear (MORS) test, where peaks appear when a group of muscle fibers/connective tissue layers has been cut and, in the case of WB meat, the blade pushed and destroyed the muscle structure instead of cutting one layer at a time. On the other hand, in agreement with the present results, other studies [
17,
48,
56] did not find a difference in shear force between WB and normal breast in the Allo–Kramer test, where cooking could reduce the differences between defective and normal meat [
54]. Nevertheless, Chatterjee et al. [
57] reported differences in some TPA traits (hardness and cohesiveness) between WB and normal breasts even after cooking, whereas in our study, the TPA analysis on cooked meat did not reveal differences according to meat type. Our findings confirm that shear force measurements on cooked meat may be more effective for discerning the texture differences between WB and SM, consistent with the findings of Pascual et al. [
48].
The chemical composition of normal breasts and breasts with myopathies are shown in
Table 2. The moisture, fat, and ash content did not differ among the meat types (
p > 0.05), whereas the presence of WB reduced protein content compared to the other meat types (
p < 0.001). Various studies have reported changes in the chemical composition of breasts with myopathies in terms of protein reduction [
13,
15,
17,
43,
58], as found in the present study for WB meat, likely due to fibrosis causing the replacement of muscle fibers with connective and adipose tissue [
13,
14,
18]. Other studies also observed reduced protein content in WS breasts [
13], whereas, in the present study, protein content was similar in WS and normal meat, as previously reported by Soglia et al. [
59] and Kuttappan et al. [
16]. Prior studies reported a link between protein reduction and WS severity [
16,
60], where the low severity of WS recorded in the present study may account for the absence of differences in chemical composition in comparison with normal meat.
Indeed, changes in protein content in WB compared to normal meat are usually within a narrow range, i.e., 1.3–3.0 percentage units [
15,
17,
40,
58], with only one study [
13] reporting larger changes (4.92 percentage units) in the protein content of WS/WB compared to normal meat. The changes observed in the present study are unlikely to have a meaningful impact on human nutrition for individuals consuming a balanced diet with a variety of protein sources, as the reduction in crude protein content is low (around 2 percentage points) and limited to WB. Additionally, Trithavisup et al. [
61] evaluated the effect of WB on in vitro protein digestibility and cytotoxicity of cooked chicken breast meat and found no differences in free-NH
2, the degree of hydrolysis, and the distribution of peptide molecular weight between normal and WB samples at late intestinal digestion, suggesting that WB has no effect on meat protein digestibility. However, the same authors suggested that further investigation is needed due to the higher WB content of peptides with oxidative modifications and reduced Caco-2 cell viability compared to normal samples, which could potentially have negative implications for human health.
In the literature, the reduction in protein content in defective meat has been accompanied by a decrease in isoleucine, leucine, and valine in WB [
18] and in arginine, leucine, lysine, methionine, phenylalanine, threonine, and valine in WS/WB breasts compared to normal breasts [
15]. In the present study, the presence of myopathies did not affect the amino acid composition (as displayed in
Table 3), with the exception of glycine. Glycine content was higher in WB (
p = 0.037), probably due to the higher content of the connective tissue rich in glycine [
62] compared to breasts from other groups.
Regarding mineral composition, as presented in
Table 4, the presence of myopathies had no impact on breast micro- and macro-element content (
p > 0.05). However, some studies reported an alteration in mineral composition in breast meat affected by muscle abnormalities. Increased levels of calcium, sodium, and iron and reduced levels of potassium, magnesium, and phosphorus have been previously reported in WS breasts [
13,
50]. Moreover, WB breasts have shown lower levels of phosphorus and potassium and higher levels of aluminum, calcium, iron, sodium, and sulfur, while elevated levels of calcium and sodium were found in SM breasts compared to unaffected muscles [
18]. In the present study, even if no significant differences in mineral content were found among the groups, Na content tended to increase from normal to WB fillets. Alteration in Na and Ca homeostasis likely has an impact on WB development [
20,
63], as, subsequent to the initial degeneration, the impairment of the sarcoplasmic reticulum results in an increased influx of calcium ions and the activation of calcium-dependent proteases, initiating myofiber necrosis [
64].
Although none of the myopathies in the present study affected total fat content, the WB meat displayed some changes in fatty acid composition compared to the WS, SM, and normal breasts. As presented in
Table 5, compared to the normal meat and SM, WB meat exhibited higher rates (
p < 0.05) of C18:2
n6 (+12.8% and +14.2%, respectively), C22:6
n3 (+18.7% and +33.3%),
n3 PUFA (+19.8% and +22.2%),
n6 PUFA (+13.0% and +13.9%), and total PUFA (+13.6% and +14.6%), with the WS samples showing intermediate (
p > 0.05) values. In addition, the rate of C18:3
n6 was higher in WB meat than in normal meat (+24.6%;
p < 0.01).
The suggested mechanisms for these results [
17] are the presence of inflammatory cells with a relatively high proportion of arachidonic acid in their membrane phospholipids [
65] or the tendency of fiber type switching from fast, glycolytic IIB fibers, in which lipids are generally more saturated, to those within slow and oxidative fibers [
64,
66]. There was a higher linolenic (ALA) and γ-linolenic (GLA) acid content in the WB breasts and a higher γ-linolenic acid content in the WS breasts compared to normal breasts in the present study, which could be due to inflammatory processes. Specifically, linoleic acid acts as a precursor to γ-linolenic acid and then arachidonic acid, the dominant substrate for proinflammatory eicosanoids synthesis [
67]. Previous studies also reported increased linolenic and α-linolenic acid [
16,
17,
43] content and total
n − 3 and
n − 6 fatty acids [
17] in breasts affected by WB and WS myopathies, which is linked to sarcolemma damages and inflammatory processes. Consistent with our results, Soglia et al. [
43] found no difference in MUFA content between WB, WS/WB, and normal breasts, whereas they reported a decrease in SFA content in muscles with abnormalities.
Further, as presented in
Table 6, the differences in the nutritional indexes were not significant among the groups (
p > 0.05), with the exception of the unsaturation index that differed between SM and WB meat (102 vs. 109;
p = 0.05). The unsaturation index did not differentiate between
n − 3 and
n − 6 fatty acids, making it less specific for nutritional evaluation but important for assessing oxidative stability [
68], where WB-affected breasts were likely more susceptible to lipid oxidation during storage.
Regarding oxidative changes, MDA (
p = 0.239) and carbonyl contents (
p = 0.541) did not differ between normal meat and meat with WS, WB, and SM, nor among the defective meat samples, as presented in
Figure 1. In this context, although no significant differences in lipid oxidation were found, the TBARS content was numerically higher in WB meat compared to normal meat and meat affected by WS and SM, likely due to somewhat increased PUFA portions. Other studies [
43,
69] reported WB presence promoting lipid oxidation in muscles due to the accumulation of reactive oxygen species and oxidative stress.
As reported in
Table 7, the sensory attributes did not differ according to the presence of myopathies (
p > 0.05). The results of the present study are the first related to SM and show no difference in sensory attributes compared to normal or WS and WB meat. Tasoniero et al. [
50] did not find differences concerning the perception of odor, strange taste, taste (sourness, bitterness, and aroma intensity), and juiciness between normal breasts and WS and WS/WB breasts; however, they did report an increase in the overall intensity of off-odors compared to normal breasts. On the other hand, several authors have reported significant detrimental effects of WB on texture, including increased hardness, as perceived by panelists [
70,
71]. In our study, these differences only approached statistical significance (
p = 0.097). This does not imply a negative result per se, as Brazilian consumers preferred moderate and severe WB levels based on the taste, softness, juiciness, and chewiness of meat compared to normal breasts [
53], suggesting that the effects of myopathies on final meat quality are also dependent on consumer preferences.
The inconsistency in results across studies may be attributed to differences in the severity of myopathies, the cooking processes applied, and sampling procedures, as certain structural changes and collagen deposition affect only the superficial muscle layers, whereas profound parts of the muscles remain intact [
70,
71,
72]. In fact, Xing et al. [
73] did not report a difference in sensory acceptance between raw normal and mild WB meat, whereas moderate and severe WB fillets affected the sensory evaluation of consumers owing to their impaired general appearance, texture, and drip losses, suggesting that the effect of WB is related to its grade (severity). Additionally, some authors [
70,
71] found that the effect of WB on meat sensory quality is not uniform throughout the breast and that the sensory attributes of springiness, hardness, and fibrousness were perceived differently between the ventral and dorsal sections of cooked WB breast meat.