1. Introduction
Consumer demands on the meat industry are increasing. In addition, the controversies that have arisen in recent years in connection with red meat indicate that there is still a need to understand the influence of various factors on its quality as well as its health value [
1,
2]. In addition to beef or pork, this also applies to lamb meat, which, due to its low production, has to comply more with quality standards in order to remain competitive in the market.
Many studies have shown that breed, age at slaughter, the feeding system and related muscle development and the proportion of different types of muscle fibers determine important meat characteristics for the consumer, such as color, tenderness, juiciness or intramuscular fat content, as well as the presence of biologically active ingredients [
3,
4,
5,
6,
7,
8,
9,
10,
11]. The quality of the meat is also affected by physiological, biochemical and metabolic changes that occur during meat aging. These changes mainly involve a drop in pH, degradation and oxidation of myofibrillar proteins, the chemical state of myoglobin, production of heat shock proteins and apoptosis, which eventually affect tenderness, color or water holding capacity (WHC) [
12,
13,
14]
The basic components of skeletal muscle are different types of muscle fibers, the conversion of which can affect both the quality of meat and the composition of bioactive compounds [
9]. To the bioactive compounds found particularly in red meat, especially in ruminants, carnosine, anserine, taurine, L-carnitine, omega-3 polyunsaturated fatty acids as well as conjugated linoleic acid isomers (CLA) are included. These compounds which are characterized by their properties that inhibit oxidative stress, inflammation as well as cancer processes, play a key role in the human body by ensuring health and proper metabolic processes. They are not always synthesized in sufficient quantities, and could be supplemented by a proper diet including red meat [
15,
16].
It has been established that in mammals, approximately 99% of carnosine is found in skeletal muscles and more in white muscles than in red ones [
17,
18]. Joo et al. [
19] found that intramuscular fat content (IMF) and the proportions of saturated fatty acids (SFA) and monounsaturated fatty acids (MUFA) in steers were correlated with the proportion of different muscle fibers. Taurine, which is now recognized as an ingredient that plays a major role in human physiology and nutrition, is found in 70% of skeletal muscle. The ability to synthetize this β-amino acid by humans is very low compared to livestock like cattle or sheep [
15]. Providing this component through the diet and sometimes even its supplementation can effectively counteract the occurrence of cardiovascular, digestive, endocrine, immune, muscular or neurological disorders [
20,
21,
22]. The L-carnitine content of lamb meat, which is involved in energy metabolism, can also depend on the type of muscle and the proportion of different muscles fibers. According to Shimada et al. [
23] in their studies conducted on hens, muscles with a higher content of oxidative and oxidative-glycolytic fibers had a higher L-carnitine content.
The aim of this study was to analyze the physicochemical characteristics and content of selected bioactive compounds (carnosine, taurine and L-carnitine, CLA) in fresh and at 7 and 14 days post-slaughtered aged lamb meat with regard to muscle type.
4. Discussion
The acceptable pH range for sheep meat should have a range between 5.5 - 5.8 [
30]. In this study, such pH values were not exceeded by both fresh and aging meat in GM and LL muscle (
Table 1). No differences in pH values between fresh meat and meat after 7 days of aging, as in the present study, were reported by Abdullah and Qudsieh [
7] in
semitendinosus, semimembranosus, biceps femoris and
longissimus muscles in Awassi sheep meat. Conversely to the obtained results, a marked decrease of pH at 7 days post-slaughter in muscle
longissimus dorsi and
semimembranosus in adult sheep was recorded by Yaner and Yetim [
31]. Decreasing pH values in lamb meat with aging up to 35 days were recorded by Gramatina et al. [
13] in a study comparing the quality of beef, lamb and pig meat. A significant reduction of this parameter, but during 0 and 24 hours after slaughter, was recorded by Yang et al. [
11] in LT muscle of Sunit sheep, which the authors explained by the accumulation of lactic acid during the process of anaerobic glycolysis. In this studies, there was no effect of muscle on the pH value either in fresh meat and after 7 and 14 days of aging. Similarly, no differences in the value of this parameter between muscles were recorded by Purchas and Zou [
32] when examining
longissimus and
infraspiratus muscle in fresh meat in cattle.
Color is a key indicator of meat quality for consumers, who consider meat color to be the main criteria for judging whether meat is fresh or not, which does not go unchallenged in the decision to buy it [
33]. One of the factors influencing changes in meat color may be the storage method and aging period [
11] The darkening of meat expressed by a higher saturation of readness and an increase in Chroma values in
gluteus medius muscle along the aging period obtained in the present study was confirmed by Yang et al. [
11] analyzing changes in quality parameters in lamb meat from 0 to 96 hours. Likewise, Abdullach and Qudsieh [
7] reported a significant increase in a* value with a slight decrease in L* value after 7 days aging of meat compared to fresh meat in Awassi lambs. The aging of meat after slaughter can increase the conversion of myoglobin to oxymyoglobin and make the muscles acquire oxygen more easily, making them redder. The observed small changes in the L* value representing the lightness of color in the conducted studies, according to McKenna et al. [
34] and Suman and Joseph [
35], do not have a great significance in stabilizing the color of red meat.
The concentration of myoglobin in skeletal muscle, which is responsible for changes in meat color, can also be affected by the type of muscle fiber [
33]. In muscle with a higher proportion of oxidative slow-contracting fibers, myoglobin content is higher than in muscle with a predominance of glycolytic fast-contracting fibers [
36]. According to Ithurralde et al. [
37], the Type I fiber content of the
gluteus medius muscle is higher than in the
longissimus lumborum. Whereas, Joo et al. [
19] determined a similar proportion of Type I fibers in GM and LL, but also indicated a significantly higher proportion of oxidative-glycolytic fast-contracting fibers (Type IIA) in
gluteus medius muscle than in LL muscle. The differences in L*, b* and Hue values between fresh muscle and in L* values after 7 days of aging can be explained by the different proportion of muscle fibers in the studied muscle types (
Table 1).
The effect of muscle type on meat color was not recorded by the authors in their previous study on Polish Merino lambs in fresh meat, while after 14 days of aging, the L* value in
longissimus lumborum muscle was significantly higher compared to GM muscle [
38]. However, in another study conducted by the authors on fresh meat from Polish Merino lambs and Polish Merino x Berrichone du Cher crossbred lambs, higher L*, lower b* and H* values were determined in the GM muscle of both tested genotypes [
5]. The variation in the values of parameters determining meat color was also indicated by Realini et al. [
39] when analyzing the relationship between meat quality and muscle type and their morphological structure in pigs.
The water holding capacity, referred to as free water, is an important indicator for assessing meat quality, as it can directly affect the juiciness, tenderness or color of meat [
40]. The lower expressed juice value in aging meat in both muscles obtained in the present study was also found by the authors in their earlier study comparing fresh meat and after 14 days of aging [
38]. A lower value for this parameter in
semitendinosus, semimembranosus, biceps femoris and
longissimus muscles in Awassi sheep after 7 days of aging was also determined by Abdullah and Qudsieh [
7]. Many factors can affect water loss including hydrolysis and oxidation of cytoskeletal proteins or cell membrane permeability. During aging, contraction of the myofibrillar reticulum and myocytes and degradation of proteins leads to relaxation of the sarcomere structure so that water retention in muscle may increase [
14,
41]
In this study, no differences in water loss were registered between muscles (
Table 1). Different results were obtained by Purchas and Zou [
32] comparing the quality of beef in the two muscle types, where the
infraspinatus muscle had a significantly higher water loss than the
longissimus muscle.
The aging time and type of muscle were not unaffected on the basic chemical composition of the meat (
Table 2). The effect of meat aging on water content found in this study in LL muscle at 7 days after slaughter was also reported by Ablikim et al. [
8] in meat from Chinese sheep breeds but after 15 days of freezing storage. In contrast, Abdullah and Qudsieh [
7] found no effect of aging time on the water content of various muscles of Awassi lambs similarly to the GM muscle in the present study. The 14-day aging period had a significant effect on the total protein content of both tested muscles, while a higher fat content after aging was recorded only in the GM muscle, which also differs from the LL muscle in terms of this parameter in meat after 7 days of aging (
Table 2). Abdullah and Qudsieh [
7] did not confirm differences in protein content of different muscles according to aging and, inversely to the present study, they also did not show differences in fat content. The research of the above-mentioned authors was consistent with previous studies conducted on fresh meat and after 14 days of aging of Polish merino lambs by Rant et al. [
38]. No differences regarding fat content between muscle types in fresh meat and after 14 days of aging, for fresh meat were also confirmed by Ablikim et al. [
8] for
longissimus dorsi and
gluteus medius muscles and by Esenbuga et al. [
4] comparing
longissimus dorsi, semitendinosus and
triceps brachi muscles in Awassi sheep. The effect of muscle type on water, protein and fat content in Blonde Galician cattle was also not observed by Franco et al. [
42].
In this study, a 7-day aging period had an effect on increasing (
p<0.05) the collagen content but only in the muscle
longissimus lumburum, differences in the proportion of this component also related to the type of muscle. More collagen was recorded in LL muscle than GM muscle at both aging periods. In the authors’ earlier study, higher collagen content in fresh meat was also found in the
longissimus dorsi muscle of both Polish Merino lambs and Merino x Berrichone du Cher crossbreds lambs compared to GM muscle [
5]. Similar to the present study, Ablikim et al. [
8] observed a higher collagen content in the
longissimus dorsi muscle compared to the GM muscle in Chinese sheep. In contrast, a higher proportion of collagen in goose breast muscle after 14 days of aging than in fresh meat was determined by Geldenhuys et al. [
43]. Differences in the content of this component depending on the type of muscle may be influenced by differences in the amount of intramuscular fat. An increase in fat can decrease collagen content, which was also observed in the present study [
44]
Although the study found no significant differences in the content of SFA, MUFA, PUFA fatty acid groups and in the content of the main isomer of C18:2 cis-9, trans-11 linoleic acid either between fresh and aging meat or between the muscles studied, it should be noted that meat after aging in both GM and LL muscles was characterized by an increase in SFA content and a decrease in MUFA and PUFA (
Table 3). A similar variation in fatty acid content during aging was obtained by Yang et al. [
11] in a study of
m.l.d. muscle in Sunit sheep subjected to different feeding regimes. As reported by Han et al. [
45] the increase in SFA may have been due to the destruction of long-chain PUFA. Due to the presence of double bonds in the structure of polyunsaturated fatty acids, they are the initiators of lipid oxidation. The oxidative stability of meat can be significantly affected by even small changes in the concentration of these acids [
46]. Thus reduction in MUFA and PUFA which are precursors of flavor during the aging of meat in the present study may be due to their easier oxidation. This is consistent with the increase (
p<0.05) in TBARS values with the aging period of the meat observed in both types of muscles (
Table 3). The higher degree of lipid oxidation expressed by a higher TBARS value in
gluteus medius muscle than in LL muscle could be explained by a higher intramuscular fat content in GM, although the differences in this component were not significant. Greater lipid oxidation was also observed in cattle meat with higher fat content [
47,
48]
The studied bioactive compounds L-carnitine, carnosine or taurine being substrates in chemical reactions occurring during thermal processing of meat, can be correlated, similarly to fatty acids, with its taste and aromatic qualities. In addition to its antioxidant, metal ion chelating or anti-glycation effects, carnosine has been attributed to its association with umami flavor [
49]. In addition, the above-mentioned metabolites during meat aging are involved in processes such as glycolysis, the Krebs cycle, protein degradation or fatty acid metabolism, which can result in a change in their content.
The decrease in carnosine and increase in L-carnitine with aging of the meat obtained in their study (
Table 4) was not confirmed by Bischof et al. [
50] when examining non-aging and aging beef for 7 and 14 days. Carnosine content increased with aging of the beef, while L-carnitine remained at similar levels in both fresh and aged meat. On the other hand, in a study by [
51] comparing metabolic changes in beef subjected to different aging treatments over a 4-week period, they observed in dry aging an initial increase in carnosine content, followed by a decrease after 14 days of aging and a renewed increase and decrease on days 21 and 28 of the study, respectively. The taurine content of the aforementioned studies decreased after 14 days of aging the meat, followed by an increase after 28 days. In present study, a decrease in taurine content occurred after 7 days of aging and increased after 14 days (
Table 4). Carnitine, as in the present study, increased due to aging, but only up to the first week, thereafter the levels of this component were stable [
51]. Carnitine, which is associated with utilizing fatty acids and facilitating their removal from the mitochondria, can be synthesized from lysine and methionine. Thus, its increase during meat aging can be linked to the release of amino acids during processes associated with protein degradation [
52].
The differences in taurine, carnosine and L-carnitine content by muscle type recorded in this study can also be seen in other authors’ studies. The lower content of taurine in the muscle of the
longissimus lumborum and the higher content in the muscle of the GM and, conversely, the higher content of carnosine in the LL and the lower content of this compound in the GM obtained in the present study (
Table 4) were confirmed in an earlier study by the authors conducted on fresh meat from Polish Merino lambs [
5].
A higher carnosine and lower taurine content in LL muscle compared to GM was also reported in lamb meat by Purchas et al. [
53]. Glycolytic fast-contracting muscle fibers (type IIB), which are more abundant in
longissimus muscle, have a significantly higher carnosine content compared to oxidative slow-contracting fibers due to their susceptibility to acidification and higher buffering capacity, as confirmed in beef by Ruiz et al. [
42] and in pork by Aristoy and Toldra [
54]. Also, a higher carnosine content in breast muscle than in thigh muscle in the control group of broilers was determined by Kralik et al. [
55] in a study of poultry meat quality in relation to the use in nutrition β-alanine and L-histidine supplementation.
A significantly higher L-carnitine content in muscle
gluteus medius compared to LL was only registered in meat after 14 days of aging (
Table 4). A higher L-carnitine content in GM also in fresh meat was determined by the authors in earlier study in Polish Merino x Berrichone du Cher crossbred lambs [
5]. Muscles with more oxidative or oxidative-glycolytic fibers may have a higher content of this component due to its association with oxygen metabolism. The higher L-carnitine content in GM may be explained by the fact that there is a high concentration of lipid compounds in red muscle, in the metabolism of which L-carnitine is involved. A higher proportion of L-carnitine in the red muscle of m. soleus in laying hens was confirmed in their study by Shimada et al. [
23].
5. Conclusions
The results of the study indicate that the aging process affected some of the physico-chemical characteristics of lamb meat. Meat after 7 and 14 days of aging was characterized by a more saturated red color, especially in muscle gluteus medius. Aged meat was also characterized by a better ability to hold own water. The aging process resulted in an increase in fat and protein content in GM muscle, while in LL muscle, in addition to an increase in protein content, collagen content also increased. After 7 days of aging the meat, the muscles differed in their basic chemical composition. In fresh meat, the chemical composition in both muscles was similar.
There were no differences in the content of SFAs, MUFAs and PUFAs and C18:2 cis-9, trans-11 according to either aging time or muscle type. The differences were in the degree of lipid oxidation. The TBARS value indicated higher levels of oxidation in aged meat and better oxidative stability in LL muscle.
As the meat aged, the L-carnitine content increased in both muscles while the GM muscle showed a higher content of this component after 14 days of aging than LL. Carnosine content, after 7 days of aging, decreased in both GM and LL, while taurine content, after a periodic decrease during the later aging period, increased, whereby the level of this component increased in both muscles. The gluteus medius muscle contained more taurine in fresh and aged meat and L-carnitine in meat after 14 days of aging while the proportion of carnosine in fresh meat was significantly higher in longissimus lumborum muscle.
In summary, it can be concluded that, due to the processes involved in turning muscle into meat, both the aging time and the type of muscle have an impact on the physico-chemical characteristics and the content of bioactive compounds.