Meat Science 90 (2012) 139–144
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Effect of season on contractile and metabolic properties of desert camel muscle (Camelus dromedarius) O.M.A. Abdelhadi a,⁎, S.A. Babiker b, B. Picard c, C. Jurie c, R. Jailler c, J.F. Hocquette c, B. Faye d a
Dept. of Animal Production, Faculty of Natural Resources & Environmental Studies, University of Kordofan, Sudan Dept. Meat Production, Faculty of Animal Production, University of Khartoum, Sudan INRA, UR1213, Herbivore Research Unit, 63122 Theix, France d CIRAD, UR 18, Campus International de Baillarguet, 34398 Montpellier cedex 5, France b c
a r t i c l e
i n f o
Article history: Received 17 June 2010 Received in revised form 25 May 2011 Accepted 10 June 2011 Keywords: Desert camel Metabolic activity Myosin heavy chain isoforms Season
a b s t r a c t Thirty fattened one humped desert camels were used to examine the effect of season on contractile and metabolic properties of Longissimus thoracis (LT) muscle. Ten camels were slaughtered according to seasons of the year (winter, summer and autumn). Season significantly influenced muscle chemical composition, ultimate pH (pHu) and color. Activities of metabolic enzymes were higher during autumn season compared to summer and winter for phosphofructokinase (+64% compared to both seasons) and for isocitrate dehydrogenase (+35% and +145% in autumn vs. summer and winter, respectively). Quantification of muscle myosin heavy chain isoforms by SDSPAGE electrophoresis showed only presence of type I and type IIa MyHC in camel muscle and indicated high proportion in winter for type I and in autumn for type IIa with respect to other seasons. Several correlations between different MyHC proportions and enzyme activities were reported. These findings indicated that muscle characteristics in camels are influenced by season. © 2011 Elsevier Ltd. All rights reserved.
1. Introduction Camel is a unique animal having the ability to survive and produce with low cost of feeding under harsh conditions compared to other livestock. It is a good source of meat in areas where the climate adversely affects other animal's production efficiency (Kadim et al., 2006). Traditionally, camel meat comes mostly from old males and females that are primarily kept for milk, racing, and transportation rather than for meat production. General consumers' view is that camel meat is unacceptably tough, but in fact meat from young camels has been reported to be comparable in taste and texture to beef (Kurtu, 2004). Carcass characteristics of camels were equal to those of other red meat animal species (Elgasim & Alkanhal, 1992). Chemically camel muscles had been found to have low fat content, high water holding capacity recommending camel meat as a healthy food with good processing properties (Babiker & Yousif, 1990). However, there is evidence of a great demand for fresh camel meat and for camel meat in blended meat products even in societies not herding camels (Morton, 1984; Pérez et al., 2000). Characteristics of camel and cattle meat as well as muscle fiber types had been studied by many authors (Costa et al., 2008; Kadim, Al-Hosni, et al., 2009; Kadim, Mahgoub, et al., 2009; Lefaucheur, 2010; Rose et al., 1992; Vestergaard, Oksbjerg, & Henchel, 2000). Different
⁎ Corresponding author at: P.O. Box: 716, Khartoum, Sudan. Tel.: + 249 9122 56 401. E-mail address:
[email protected] (O.M.A. Abdelhadi). 0309-1740/$ – see front matter © 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.meatsci.2011.06.012
isoforms of Myosin Heavy Chain (MyHC) in bovine muscle were described: MyHC I, MyHC IIa and MyHC IIx (Picard, Duris, & Jurie, 1998). The MyHC IIb had been reported in some cattle from the Blonde d'Aquitaine French breed (Picard & Cassar-Malek, 2009). Muscle characteristics and meat quality have been known to be affected by growth and breed type (Renand, 1990), age and sex (Monin, 1990) as well as feeding level and diet composition (Geay, Bauchart, Hocquette, & Culioli, 2001). Klont, Brocks, and Eikelenboom (1998) noted that muscle metabolic and contractile types are adaptable and may be modified in living animals by environmental conditions and genetic selection. They indicated that in cattle, environmental effects were more important due to the large variations in production methods. To our knowledge, the effect of season on camel meat characteristics has not been reported. The present work aimed to investigate the effect of seasons on muscle characteristics of one humped desert camel (Camelus dromedarius). 2. Materials and methods 2.1. Sample collection Thirty fattened, intact males of the one hump desert camel, 2–3 years of age were used in this study. Ten camels were slaughtered at each season of the year: 2008 winter (Feb.–Mar.), summer (May–June) and autumn (Aug.–Sept.). Slaughter was performed following similar routine as described in Yousif and Babiker (1989). Average live weights were 319.4, 272.7 and 232.6 kg in winter, summer and autumn, respectively.
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Mean values of temperature (°C) and relative humidity (%) were (26.5 °C, 22.5%), (35 °C, 24.5%) and (32 °C, 44.5%) in winter, summer and autumn, respectively. Muscle samples were collected immediately post-slaughter from Longissimus thoracis (LT) of the right carcass side between the 5th and 8th ribs. Samples were placed in plastic bags and transported within 60 min of slaughter to the laboratory in an insulated box filled with ice. Visible fat was trimmed from the muscles and each muscle was subsampled (approximately 5 g sample weight) at the 5th rib. Sample was chopped into small pieces (0.5 cm), immersed in liquid nitrogen and stored in well tight plastic tubes at − 18 °C for a week before transportation to INRA laboratories, France where samples were stored at −80 °C awaiting analysis of metabolic and contractile characteristics. Samples were also taken at the 6th rib for the determination of fresh muscle ultimate pH (pHu) and chemical composition. The remainder of the muscle was packed under vacuum and stored at −18 °C for the measurements of frozen meat color and pHu.
70 V for 30 h at 4 °C. The relative proportions of slow isoforms (% MyHC I) and fast isoforms (% MyHC IIa, IIx and IIb) were determined after staining of gels in a solution of Coomassie Blue R250 and quantifying using Image Quant TL v2003. 2.6. Statistical analyses Data were analyzed using Statistical Analysis Systems package (SAS, 2001) to evaluate the effect of seasons on muscle characteristics of desert camels (Camelus dromedaries). Significant differences between means were assessed using DUNCAN multiple range test. Principal Component Analysis (PCA) was used to interpret the relationship between different parameters as previously used in cattle for carcass composition (Albertí et al., 2008; Hocquette, Bas, Bauchart, Vermorel, & Geay, 1999) and meat quality (Destefanis, Barge, Brugiapaglia, & Tassone, 2000). 3. Results and discussion
2.2. Chemical composition 3.1. Chemical composition Muscle samples were ground to a homogenous mass in a grinder then used for chemical analyses. Chemical composition of the muscle tissue was measured according to standard methods of AOAC (1990). Crude protein was determined using a Foss Tecator Kjeltec 2300 Nitrogen/Protein Analyzer. Fat was determined by Soxhlet extraction of the dry sample, using petroleum ether. Ash content was determined by ashing samples in a muffle furnace at 500 °C for 24 h. 2.3. Meat color and pH Muscle color co-ordinates (L*, a* and b*) were determined after thawing of frozen samples to 2 °C as described by Allais et al. (2010) since it was not possible to measure meat color on fresh meat in Sudan. The L* value relates to lightness, the a * value to red–green hue where a positive value relates to the red intensity; and the b* value to the yellow–blue, where a positive value relates to yellow intensity. Ultimate muscle pH (pHu) was measured using a portable pH meter (Hanna waterproof pH meter, Model H I 9025, Italy) and a temperature adjusting probe. Readings were recorded in triplicates for each measurement; the pH probe and the thermometer were inserted into muscles to a similar depth (1.5 cm). 2.4. Metabolic enzyme activities The metabolic muscle type was determined by measuring enzyme activities. Glycolytic enzyme activities: phosphofructokinase (PFK, EC 2.7.1.11) and lactate dehydrogenase (LDH, EC 1.1.1.27), and oxidative enzyme activities: isocitrate dehydrogenase (ICDH, EC 1.1.1.42) and cytochrome-c oxidase (COX, EC 1.9.3.1) were measured spectrophotometrically, according to the methods and the detailed protocols cited by Jurie, Ortigues-Marty, Picard, Micol, and Hocquette (2006). One unit of the enzyme was defined as the amount which catalyzes per min the disappearance of 1 μmol of NADH for PFK and LDH, the reduction of 1 μmol of NADP for ICDH and the oxidation of 1 μmol of cytochrome-c for COX. Enzyme activities (means of triplicate) were expressed in μmol per min per gram of wet muscle (μmol/min per g muscle).
The overall chemical composition of Longissimus thoracis muscle showed mean values of 76.9, 23.1, 17.2, 2.6 and 1.6% for moisture, dry matter, crude protein, intramuscular fat and ash content, respectively. Generally the mean values of chemical composition in the present work were within the range reported previously for moisture (70–77%), crude protein (20–23%), fat (0.5–9.8%) and ash (1–1.3%), for LT muscle of 1–3 years old camels (Al-Ani, 2004; Al-Owaimer, 2000; Al-Sheddy, AlDagal, & Bazaraa, 1999; Babiker & Yousif, 1990; Dawood & Alkanhal, 1995; El-Faer, Rawdah, Attar, & Dawson, 1991; Kadim et al., 2006; Kadim & Mahgoub, 2006; Kadim, Mahgoub, et al., 2009; Kadim, Mahgoub, Al-Marzooqi, Al-Maqbali, & Al-Lawati, 2008; Kamoun, 1995). No significant differences were found among seasons for moisture, dry matter and intramuscular fat content in camel LT muscle (Table 1). However during winter season both crude protein and ash were either lower or significantly lower than values for summer and autumn seasons. The decrease in crude protein and ash during winter might be due to nutritional factors as winter feed requirements are higher than that of the other seasons. Crude protein values of camel LT muscles during the different seasons of the year were slightly lower (17.2%) than values earlier reported by Babiker and Yousif (1990) for desert camels in the same region (21.6%), as well as Dawood and Alkanhal (1995), Kamoun (1995), Al-Sheddy et al. (1999), Kadim et al. (2006) and Kadim, Mahgoub, et al. (2009) gave crude protein values of the camel LT muscles of 20.0, 18.7, 21.3, 22.7 and 21.6%, respectively. Ash content was significantly higher in autumn than in summer and winter (1.8 vs. 1.5 and 1.4%, Table 1) and almost similar to that reported by Babiker and Yousif (1990) and Kadim, Mahgoub, et al. (2009). In general, camel meat is high in moisture content, moderate in protein and ash, but low in fat, which clearly confirms the fact that camel meat is healthier due to its low intramuscular fat content compared to other species (for review, see Hocquette et al., 2010) like cattle (Chambaz, Scheeder, Kreuzer, & Dufey, 2003; Delgado et al., Table 1 Effect of season on chemical composition of Longissimus thoracis muscle of desert camel. Parameter (%)
2.5. Contractile characteristics of LT muscle The contractile muscle type was determined by quantifying the different myosin heavy chain (MyHC) isoforms by electrophoresis SDS-PAGE according to the method of Talmadge and Roy (1993) and adapted for bovine muscle by Picard, Barboiron, Chadeyron, and Jurie (2007). Each hole of gel was loaded with 4–5 μg of myofibrillar protein and electrophoresis was performed at a constant voltage of
Season
S.E
Winter Summer Autumn Moisture 76.7 Dry matter 23.3 Crude protein 16.8b Intramuscular fat 2.7 Ash 1.4b
76.8 23.2 17.3a 2.5 1.5b
77.3 22.7 17.5a 2.6 1.8a
Overall Effect of mean season (P-value)
0.26 76.9 0.27 23.1 0.08 17.2 0.17 2.6 0.05 1.6
0.82 0.82 0.0002 0.87 0.0002
SEM = Standard error of the mean and Overall = Overall mean of the three seasons. a,b means with different superscripts within a row are significantly different (P b 0.05).
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2005; Sasaki, Mitsumoto, & Kawabata, 2001), sheep (Farid, 1991; Sen, Santra, & Kadim, 2004) and goats (Gaili & Ali, 1985; Mahgoub, Kadim, Al-Saqry, & Al-Busaidi, 2004; Sen et al., 2004).
IIb
3.2. Muscle pH and color
I
Table 2 shows the effect of season on muscle pHu and color of camel LT muscle. Muscle pHu values determined in fresh and thawed samples were almost identical, only the later were included in the table. The mean value pHu was 5.8 which falls within the pHu range value of 5.4–6.0 reported by Kadim and Mahgoub (2006), Shariatmadari and Kadivar (2006), Kadim et al. (2006, 2008) and Kadim, Mahgoub, et al. (2009) for camel Longissimus dorsi muscle at 1–3 years of age. Muscle pHu in the present work was significantly higher in autumn than in winter or summer respectively (6.03 vs. 5.7 and 5.8, P = 0.002). This suggests that the muscle tissue may have low stored muscle glycogen during autumn due to a slight higher (but not significant) moisture content of the meat during this season. Soltanizadeh, Kadivar, Keramat, and Fazilati (2008) and Kadim et al. (2006) indicated that camels have higher pH values compared to bovine especially in young ages due to slow/or low level of stored glycogen. The overall mean values of L*, a* and b* were 34.0, 13.2 and 11.2, respectively. The L*, a* values were lower while the b* values were higher than that reported by Kadim et al. (2006), Kadim, Mahgoub, et al. (2009) and Kadim, Al-Hosni, et al. (2009) for camel LT muscle. These differences could be attributed to breed differences. Between seasons, significant differences were observed in a* (P = 0.03) and b* values (P= 0.0001), while, no significant differences were observed in L* values. The b* values were significantly lower in autumn than in summer and winter (9.4 vs. 12.9 and 11.3), and a* values were significantly higher in autumn (14.6) than summer (11.8). These findings indicated that camel meat color was variable between seasons. It was significantly darker red in autumn than in summer and less yellow in autumn than in summer and winter. Young, Seok, Young, and Sung (2003) found significant effect of seasons on color and pH of LT muscle in cattle: The L*, a* and b* values were significantly lower (Pb 0.05) for cattle slaughtered in winter compared to summer, autumn and spring. In contrast, Kadim et al. (2004) found significant increase in L*, a* and b* values in bovine during cold season compared to hot season. They concluded that season had a significant effect on meat quality characteristics of beef LT muscle: ambient temperatures of approximately 35° C had increased the ultimate pH and resulted in darker meat color (L*, a*and b* reduced). Camel LT muscle is characterized by more redness and less yellowness in autumn than in the other seasons of the year which make the meat dark red in color during this season. 3.3. Contractile characteristics of LT muscle The separation of different MyHC isoforms by electrophoresis SDSPAGE revealed two MyHC isoforms (MyHC I and MyHC IIa) in camel LT muscle (Fig. 1). The fast isoforms (MyHC IIx and MyHC IIb), described in bovine muscle (Picard & Cassar-Malek, 2009) and found in bovine Table 2 Effect of season on muscle pHu and color values of Longissimus thoracis muscle of desert camels. Parameter
Season Winter
pHu Muscle color L* lightness a* redness b* yellowness
S.E. Summer
5.7b
5.8b
34.6 13.3ab 11.3a
34.9 11.8b 12.9a
Autumn 6.03a 32.6 14.6a 9.4b
Overall mean
Effect of season (P-value)
0.24
5.8
0.002
0.45 0.68 0.35
34 13.2 11.2
0.32 0.03 0.0001
SEM = Standard error of the mean, Overall = Overall mean of the three seasons. a,b means with different superscripts within a row are significantly different (P b 0.05).
IIx IIa
Winter
Summer
Autumn
B
C
A Fig. 1. Separation of different myosin heavy chain (MyHC) isoforms of Longissimus thoracis muscle of the camel and bovine by electrophoresis SDS-PAGE. A = Longissimus thoracis of camels, B = Longissimus thoracis of bovine, and C = Diaphragm of bovine. I, IIa, IIx and IIb are myosin heavy chain isoforms.
LT muscle were taken as a reference for our electrophoresis (Fig. 1), but they were not revealed in any of the camel LT samples. This result fits with the absence of IIX (fast glycolytic) fibers in camel LT in the present study. The proportions of the MyHC I and MyHC IIa isoforms were significantly modified with season (P = 0.0001), (Table 3). The MyHC I percentage was the highest in winter (85.2), least in autumn (52.9) and intermediate in summer (65.4), and inversely the MyHC IIa percentage was least in winter (14.8), highest in autumn (47.1) and intermediate in summer (34.6). The fiber types differ in MyHC isoforms among muscles. The major MyHC isoforms (slow MyHC I or fast MyHC IIa, IIx and IIb) determine the contractile activity of muscle fibers. So slow MyCH I and fast MyHC IIa, IIx and IIb were reported to be expressed in type I and type IIA, and type IIX and IIB fibers, respectively. In addition, the types of muscle fibers can be classified on the basis of their contractile and metabolic activities. The common classification involves slow twitch oxidative (SO, type I), fast twitch oxidative glycolytic (FOG, type IIA) and fast twitch glycolytic (FG, type IIX and type IIB) fiber types. Consequently slow fibers have a higher oxidative activity as they are able to use mainly fatty acids as energyyielding nutrients. Unlike this study, the presence of type IIB muscle fibers (or FG fibers) has been reported by Kadim, Mahgoub, et al. (2009) and Kadim et al. (2004) in LT muscle of camels. This discrepancy can be explained by the fact that these authors used histochemistry to assess both the contractile and metabolic properties of muscle fibers unlike in our study in which we assessed myosin heavy chain proportions only. A recent work indicated that a classification based on ATPase and SDH activities may not be always appropriate, since FOG fibers may have no SDH activity and may be confused with FG fibers (Oury, Dumont, Jurie, Hocquette, & Picard, 2010). The overall mean percentages of type I and type IIa fibers in the present study were 67.8 and 32.2%, respectively. In the present work, it was observed that the proportion of type I fibers were higher than type IIa among seasons, which is generally in line with the results of Kadim, Mahgoub, et al. (2009) who observed a higher proportion of type I (33.1%) compared to type IIa (25.2%). Rose et al. (1992) also reported a higher proportion of type I compared to type IIa muscle fibers in racing camels during resting time with an average of 70.3 and 28.0%, respectively. In contrast, Kadim, Al-Hosni, et al. (2009) found a low proportion of type I vs. types IIa and IIb (29.9 vs. 40.1 and 29.9)%, respectively, in LT muscle of 1–3 years old camels, while Kassem, El-Sayed, and Ahmed (2004) reported mean percentages of 14.5%, 46.7% and 38.8% for types I, IIa and IIb fibers in LT muscle of 2 years old camels, respectively. In addition to breed differences, genotype and seasonal ambient temperature were reported to affect muscle biochemical characteristics (Gondret, Combes, Lefaucheur, & Lebret, 2005; Gunning & Hardeman, 1991; Pette & Staron, 2001). The decrease in the proportion of type I MyHC isoforms (from 85.2 in winter to 52.9% in autumn) is associated with an increase in type IIa MyHC isoforms (from 14.8 in winter to 47.1% in autumn) concomitant to high values
O.M.A. Abdelhadi et al. / Meat Science 90 (2012) 139–144
Parameters
Enzyme activity PFK LDH ICDH COX MyHC I IIa
Season
S.E.
Overall mean
Effect of season P-value
Winter
Summer
Autumn
1.1b 256 1.1c 5.6b
1.1b 254 2.0b 10.9a
1.8a 246 2.7a 9.6a
0.16 18.3 0.19 1.13
1.3 252 1.9 8.8
0.008 0.93 b.0001 0.008
85.2a 14.8c
65.4b 34.6b
52.9c 47.1a
2.8 2.8
67.8 32.2
b.0001 b.0001
S.E = Standard error of the mean, Overall = Overall mean of the three seasons, PFK = Phosphofructokinase, LDH = Lactate dehydrogenase, ICDH = Isocitrate dehydrogenase, and COX = Cytochrome-c oxidase. a,b,c means with different superscripts within a row are significantly different (Pb 0.05).
of ICDH and COX activities in autumn (Table 3), which may suggest that oxidative activities of type IIA fibers is higher than that of type I fibers in camel muscle as described in sheep muscle (Briand, Talmant, Briand, Monin, & Durand, 1981) but not in bovine muscle (Talmant, Monin, Briand, Dadet, & Briand, 1986). It was observed that camels in the present work had small movement during winter and summer compared to autumn, which goes in line with the results of Jurie, Picard, and Geay (1998) who indicated that loose housing increased muscle oxidative metabolism as compared with tying-type housing. Vestergaard et al. (2000) also stated that the frequency of type IIa fibers were higher in bull muscles at pasture compared with tie-stall housing. 3.4. Metabolic enzyme activities Table 3 also reports metabolic enzyme activities in LT muscle of camels. Mitochondrial enzymes, both oxidative ICDH and COX activities, as well as glycolytic PFK activity significantly differed among seasons, whereas no significant differences were observed in glycolytic LDH activity among seasons. The PFK activity was almost 2 fold higher in autumn than in winter and summer [1.8 vs. 1.1 μmol/min per g muscle]. The COX activity was 2 fold lower in winter than in autumn and summer [5.6 vs. 9.6 and 10.9 μmol/min per g muscle]. The ICDH activity was significantly different among the 3 seasons, the highest in autumn (2.7), the least in winter (1.1) and intermediate in summer (2.0 μmol/min per g muscle). These differences could be attributed to variations in temperature and humidity between seasons, which would indicate a possible effect of seasonal factors on enzymes activity. The muscular metabolism in camel LT muscle is less oxidative in winter than in other seasons. To our knowledge, no studies reported any evaluation of metabolic enzyme activities in camel muscle. There is a lack of information regarding enzymes activities in camel muscle. Also Jurie et al. (2005) indicated that LDH activity in LT muscle of bulls (892 μmol/min per g muscle) was higher than the present result, while ICDH activity (1.9 μmol/min per g muscle) reported by the same authors was between summer and winter values for ICDH activity in the present study (1.1 and 2.0 μmol/min per g muscle). 3.5. Relationship among the different parameters studied
activities (PFK, LDH, ICDH), pHu, ash, protein proportions and redness on one hand, and MyHC I proportion, lightness and yellowness on the other hand, were the most important variables associated with axis 1 (PC1). As shown in Fig. 2b, PC1 discriminates the camels slaughtered in autumn (A) from those slaughtered in winter (W) and summer (S). For PC2, moisture proportion on one hand and dry matter and fat proportion on the other hand, were the most important variables associated with axis 2. PC2 discriminates between camels slaughtered in winter (W) from those slaughtered in summer (S). The PCA showed a high positive correlation (0.82) between the proportion of fiber type IIa and ICDH activity, while medium correlation was found with LDH, PFK and COX enzyme activities (0.42, 0.53 and 0.41; P b 0.05), respectively. This confirms that type IIa fibers are intermediate in their metabolism (oxido-glycolytic), due to the strong relationship to ICDH (marker enzymes of the tricarboxylic acid cycle), COX (an enzyme of the respiratory chain) and PFK (an enzyme of glycolytic pathway). This observation is in line with the results obtained by Klont et al. (1998) and Jurie et al. (2006, 2007). The proportions of types IIa and I muscle fibers were found logically negatively correlated (Pb 0.01). On the other hand, ICDH activity was significantly correlated (Pb 0.01) with PFK and COX (0.61 and 0.54) activities respectively. In
A 1,0 Moisture%
COX
0,5
Fact. 2 : 17,02%
Table 3 Effect of season on muscle metabolic enzyme activities (μmol/min per g muscle) and percentage of myosin heavy chains (MyHC) isoforms of Longissimus thoracis muscle of desert camels.
ICDH
IIA 0,0
PFK
I
Protein% Ash% Redness Fat%
DM%
-1,0 -1,0
-0,5
0,0
0,5
1,0
Fact. 1 : 32,33%
B
5 4 3
W9
2
A5 A7 A6
0 A9
-1
W6 S2
A2
1
A12
A1
W5 W2 W8 W4 S3 W1 S1 S6 W7 S5
S7
A11 S8 S4
A10
-2
A8
-3
S10 S9
-4 -5 -6 -8
Fig. 2a, illustrates the relationship between different parameters studied: enzymes activities, fiber type, chemical composition and pHu of muscles, while Fig. 2b shows the distribution of animals according to season of slaughter. Principal component analysis (PCA) was performed to study the relationship between chemical composition, muscle pHu, meat color parameters as well as metabolic and contractile muscle characteristics (total: 14 variables). The first 2 axes in Fig. 2a explained about 49% of the total variance. MyHC IIa proportion, metabolic enzyme
Yellowness Lightness
pH LDH
-0,5
Fact. 2 : 17,02%
142
-6
-4
-2
0
2
4
6
8
Fact. 1 : 32,33% Fig. 2. Plot for the variables (Fig. 2a) and for the animals (Fig. 2b) in the multivariate space following a principal component analysis (PCA). In Fig. 2a: DM = Dry matter proportion, I = MyHC I proportion, IIa = MyHC IIa proportion, PFK = Phosphofructokinase activity, LDH = Lactate dehydrogenase activity, ICDH = Isocitrate dehydrogenase activity, and COX = Cytochrome-c oxidase activity. In Fig. 2b: A = autumn, W = winter and S = summer. 1, 2…11 = distribution of animals according to season of slaughter.
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addition, activities of PFK and LDH (another enzyme of the glycolytic pathway) were also positively correlated (r = 0.53; P b 0.01, Fig. 2a). On average, this analyses indicates that type IIa muscle fibers have a higher metabolic activity (oxidative and glycolytic) than type I fibers. The relationship between PFK and muscle pHu has been reported earlier by Trivedi and Danforth (1966), Pettigrew and Frieden (1979) and Ichihara and Abiko (1982) who indicated that PFK activity is highly sensitive and inhibited by low muscle pH in situ in rabbit, frog and canine muscles. Rhoades et al. (2005) indicated that PFK activity in bovine muscles was depressed in low pHu. These findings contrasted the present results that no significant correlation coefficient (P N 0.05) was observed between PFK enzyme and muscle pHu, although higher pHu value and PFK activity were observed in autumn compared to other seasons (P b 0.001). Significant correlation (P b 0.01) was found between pHu and ICDH (0.59). No significant relationship was observed in the present findings between pHu, or LDH with color (L*, a*, and b*) values. This contrasts with the results of Mancini, Kim, Hunt, and Lawrence (2004) who reported that LDH is involved in regeneration of postmortem NADH from lactate and, consequently, in metmyoglobin reduction which diminishes redness of meat. However, the correlations between PFK and L* on one hand, and a* values were − 0.26 and + 0.43, respectively, which indicated that camel meat color was brighter and less red when PFK activity (i.e. glycolytic metabolism) was high. This fits with the findings reported by Cuvelier et al. (2006) in bovine LT muscle who indicated that bovine meat was redder when COX activity (i.e. oxidative metabolism) increased and brighter when LDH activity (i.e. glycolytic metabolism) was high. Significant correlation coefficient was observed between pHu and ICDH (0.59, P b 0.01). The b* value was also negatively correlated (P b 0.05) with ICDH (− 0.39). In conclusion, the results from this study would indicate that muscle fiber characteristics of desert camel's Longissimus thoracis muscle as well as enzymes activities could be influenced by seasonal factors. The study also revealed that the season has a significant effect on chemical composition of LT muscle (ash and protein), as well as meat color in terms of a* and b* values. Acknowledgments The chemical analysis at INRA-Theix, France was funded by the French embassy at Khartoum, Sudan. Thanks are extended to Christiane Barboiron and David Chadeyron from Herbivore Research Unit (INRA-Theix, France) for their assistance in the lab. References Al-Ani, F. K. (2004). Use and production of camels. In F. K. Al-Ani (Ed.), Camel management and diseases (pp. 91–114). (1st ed.). : Al-Sharq Printing Press. Albertí, P., Panea, B., Sanudo, C., Olleta, J. L., Ripoll, G., Ertbjerg, P., et al. (2008). Live weight, body size and carcass characteristics of young bulls of fifteen European breeds. Livestock Science, 114, 19–30. Allais, S., Leveziel, H., Payet, N., Hocquette, J. F., Lepetit, J., Rousset, S., et al. (2010). The two mutations Q204X and nt821 of the myostatin gene affect carcass and meat quality in heterozygous young bulls of three French beef breeds. Journal of Animal Science, 88, 446–454. Al-Owaimer, A. N. (2000). Effect of dietary Halophyte Salicornia bigelovii Torr on carcass characteristics, minerals, fatty acids and amino acids profile of camel meat. Applied Animal Research, 18, 185–192. Al-Sheddy, I., Al-Dagal, M., & Bazaraa, W. A. (1999). Microbial and sensory quality of fresh camel meat treated with organic acid salts and/or bifidobacteria. Journal of Food Science, 64, 336–339. AOAC (1990). Official methods of analysis (15th Ed.). Arlington, VA, USA: Association official Analytical Chemists. Babiker, S. A., & Yousif, O. Kh. (1990). Chemical composition and quality of camel meat. Meat Science, 27(4), 283–287. Briand, M., Talmant, A., Briand, Y., Monin, G., & Durand, R. (1981). Metabolic types of muscle in the sheep. 1. Myosin atpase, glycolytic, and mitochondrial enzymeactivities. European Journal of Applied Physiology and Occupational Physiology, 46, 347–358. Chambaz, A., Scheeder, M. R. L., Kreuzer, M., & Dufey, P. A. (2003). Meat quality of Angus, Simmental, Charolais and Limousin steers compared at the same fat content.
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