Effects of Electrical Stimulation on Histochemical Muscle Fiber Staining, Quality, and Composition of Camel and Cattle Longissimus thoracis Muscles

Authors

  • I.T. Kadim,

    1. Authors Kadim, Mahgoub, Al-Marzooqi, and Khalaf are with Dept. of Animal & Veterinary Sciences, author Mansour is with Dept. of Soil, Water and Agricultural Engineering, College of Agricultural and Marine Sciences, and authors Al-Sinani and Al-Amri are with Dept. of Pathology, College of Medicine and Health Sciences, Sultan Qaboos Univ., P.O. Box 34, Al-Khoud 123, Muscat, Sultanate of Oman. Direct inquiries to author Kadim (E-mail: isam@squ.edu.om).
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  • O. Mahgoub,

    1. Authors Kadim, Mahgoub, Al-Marzooqi, and Khalaf are with Dept. of Animal & Veterinary Sciences, author Mansour is with Dept. of Soil, Water and Agricultural Engineering, College of Agricultural and Marine Sciences, and authors Al-Sinani and Al-Amri are with Dept. of Pathology, College of Medicine and Health Sciences, Sultan Qaboos Univ., P.O. Box 34, Al-Khoud 123, Muscat, Sultanate of Oman. Direct inquiries to author Kadim (E-mail: isam@squ.edu.om).
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  • W. Al-Marzooqi,

    1. Authors Kadim, Mahgoub, Al-Marzooqi, and Khalaf are with Dept. of Animal & Veterinary Sciences, author Mansour is with Dept. of Soil, Water and Agricultural Engineering, College of Agricultural and Marine Sciences, and authors Al-Sinani and Al-Amri are with Dept. of Pathology, College of Medicine and Health Sciences, Sultan Qaboos Univ., P.O. Box 34, Al-Khoud 123, Muscat, Sultanate of Oman. Direct inquiries to author Kadim (E-mail: isam@squ.edu.om).
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  • S.K. Khalaf,

    1. Authors Kadim, Mahgoub, Al-Marzooqi, and Khalaf are with Dept. of Animal & Veterinary Sciences, author Mansour is with Dept. of Soil, Water and Agricultural Engineering, College of Agricultural and Marine Sciences, and authors Al-Sinani and Al-Amri are with Dept. of Pathology, College of Medicine and Health Sciences, Sultan Qaboos Univ., P.O. Box 34, Al-Khoud 123, Muscat, Sultanate of Oman. Direct inquiries to author Kadim (E-mail: isam@squ.edu.om).
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  • M.H. Mansour,

    1. Authors Kadim, Mahgoub, Al-Marzooqi, and Khalaf are with Dept. of Animal & Veterinary Sciences, author Mansour is with Dept. of Soil, Water and Agricultural Engineering, College of Agricultural and Marine Sciences, and authors Al-Sinani and Al-Amri are with Dept. of Pathology, College of Medicine and Health Sciences, Sultan Qaboos Univ., P.O. Box 34, Al-Khoud 123, Muscat, Sultanate of Oman. Direct inquiries to author Kadim (E-mail: isam@squ.edu.om).
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  • S.S.H. Al-Sinani,

    1. Authors Kadim, Mahgoub, Al-Marzooqi, and Khalaf are with Dept. of Animal & Veterinary Sciences, author Mansour is with Dept. of Soil, Water and Agricultural Engineering, College of Agricultural and Marine Sciences, and authors Al-Sinani and Al-Amri are with Dept. of Pathology, College of Medicine and Health Sciences, Sultan Qaboos Univ., P.O. Box 34, Al-Khoud 123, Muscat, Sultanate of Oman. Direct inquiries to author Kadim (E-mail: isam@squ.edu.om).
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  • I.S. Al-Amri

    1. Authors Kadim, Mahgoub, Al-Marzooqi, and Khalaf are with Dept. of Animal & Veterinary Sciences, author Mansour is with Dept. of Soil, Water and Agricultural Engineering, College of Agricultural and Marine Sciences, and authors Al-Sinani and Al-Amri are with Dept. of Pathology, College of Medicine and Health Sciences, Sultan Qaboos Univ., P.O. Box 34, Al-Khoud 123, Muscat, Sultanate of Oman. Direct inquiries to author Kadim (E-mail: isam@squ.edu.om).
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Abstract

ABSTRACT:  The effects of electrical stimulation on muscle fiber type, meat quality, and composition of Longissimus thoracis muscles from one-humped camels and Dofari Omani cattle of a comparable age range were investigated. A low-voltage electrical stimulation with 90 V, 14 Hz (pulse of 7.5-millisecond duration every 70 milliseconds) 20 min postmortem was applied. Samples from the left muscle were collected from 20 (2 to 3 y) camels and 24 cattle (1 to 3 y). For chemical composition, muscle samples were dried in a freeze dryer, and then ground to determine moisture, protein, fat, and ash. Macro- and micro-minerals were determined using an Inductively Coupled Plasma Emission Spectrometer. Quality characteristics of the meat were evaluated using shear force value, pH, sarcomere, myofibrillar fragmentation index, expressed juice, cooking loss percent, and CIE L*, a*, b* color values. Electrical stimulation resulted in a significantly (P < 0.05) more rapid pH fall in the muscle during the first 24 h after slaughter in both species. Muscles from electrically stimulated carcasses had significantly (P < 0.05) lower ultimate pH, longer sarcomere, and lower shear force values than those from nonstimulated carcasses. Lightness (L*), myofibrillar fragmentation, and expressed juice were significantly (P < 0.05) higher for stimulated than for nonstimulated muscles. Muscles of camels had significantly (P < 0.05) higher expressed juice, cooking loss percent, redness color (a*), and lower fat, Mg, K, and P than those from cattle. Electrical stimulation improved quality characteristics of meat from both species. This indicates that meat quality of local camel and cattle can be improved by electrical stimulation and consequently improves their acceptability to consumers and better marketability.

Introduction

Meat is the most important and preferable product of the one-humped camel and cattle in the Sultanate of Oman. Their numbers in Oman have been estimated at 117299 and 301558 for camel and cattle, respectively, out of a total of about 2327071 livestock (MAF 2004/2005). Most of the Arabian camels and cattle are found in the southern region of Oman. Their meat production can be efficiently exploited to supply high-quality protein. Compared to other livestock, the camel is unique for having an exceptional ability to survive and thrive under adverse climatic conditions of high ambient temperatures, low rainfall, and feed scarcity. Moreover, camel produces low-fat carcasses with less cholesterol and relatively high polyunsaturated fatty acids than other livestock (Kadim and others 2008b). Camel meat is also used for remedial purposes for diseases such as hyperacidity, hypertension, pneumonia, and respiratory disease as well as an aphrodisiac (Kurtu 2004). The general public perception is that camel meat is associated with toughening and low quality characteristics compared to other red meat animal species because their meat comes mostly from old animals that are primarily kept for milk, racing, and transportation rather than for meat production (Kadim and others 2008b). Omani cattle meat is also considered tough in consumers' view.

Electrical stimulation is a proven method for improving meat quality of beef cattle (Taylor and Marshall 1980; McKeith and others 1981; Calkins and others 1983; Eilers and others 1996; Hwang and Thompson 2001; White and others 2006; Rosenvold and others 2008) and camel (Kadim and others 2008c). Applying electrical stimulation to increase the postmortem muscle metabolism and hasten the onset of rigor mortis could improve the quality characteristics of camel and cattle meat. The improvement in electrically stimulated meat was attributed to physical disruption of myofibrillar matrix or acceleration of proteolysis (Hwang and others 2003). The objective of this study was to evaluate the effect of low-voltage electrical stimulation on muscle fiber types, meat quality characteristics, and chemical composition of one-humped camel and Omani cattle Longissimus thoracis muscle slaughtered at comparable age range.

Materials and Methods

Electrical stimulation

Fifty percent of the carcasses from each species were randomly electrically stimulated using V1.3-R3B stimulator (7.5 millisecond duration every 70 milliseconds [14 Hz] and an output of 90 V, AgResearch, New Zealand), 20 min postmortem. Carcasses were stimulated for 60 s with a battery clip attached to the upper lip of the jaw and stainless steel hook contacting the Achilles tendon.

Meat samples

L. thoracis muscle samples were randomly collected from 20 male one-humped camels (2 to 3 y) and 24 Omani beef (1 to 3 y) slaughtered at Bausher slaughterhouse, Sultanate of Oman. Animals were exposed to similar routine preslaughter handling, including transportation and subsequently held in a lairage for 1 to 2 h. Animals were slaughtered and dressed following Muslim (Halal) methods. Ambient temperatures on slaughter days ranged between 25 and 27 °C. The L. thoracis muscle was removed from the left side of each carcass between the 10 and 13 ribs (800 to 1000 g) within 20 min postmortem. Samples were transported in an insulated cool box from the slaughter house to the meat lab at Sultan Qaboos Univ. and kept in a chiller (2 to 3 °C) within about 2 to 2.5 h postmortem for 48 h before running quality and composition measurements.

Muscle pH decline

The pH from the left side L. thoracis muscle was monitored using a portable pH meter (Hanna waterproof pH meter, Model HI 9025, Italy) fitted with a polypropylene spear-type gel electrode (Hanna HI 1230) and a temperature adjusting probe. Measurements, designated as pH (40 min, 1, 2, 4, 6, 8, 10, 12, 24 h postmortem) were recorded. For each measurement, the pH probe and the thermometer were inserted (1.5 cm) into muscles to a similar depth.

Histochemistry

Core samples of the right L. thoracis at the last rib location were removed immediately after electrical stimulation and cut into 1 × 1 cm pieces and immediately frozen in liquid nitrogen. Muscle samples were cut into 8-μm thickness on a cryostat (Model Bright OTF 5000, Bright Instrument Co. Ltd. Huntingdon, Cambridgeshire, U.K.) and mounted on silane-treated microscope slides. Two sections from each sample were incubated in an acetic acid (0.2 M) at pHs 4.35 and 4.60 for 10 min and then incubated at adenosine 5-triphosphate substrate pH 9.5 for 45 min. The sections were then incubated for 3 min in an aqueous cobalt chloride and a solution of ammonium sulphide. A blackish–brownish cobalt sulphide is generated in the reaction to replace cobalt phosphate (Brooke and Kaiser 1970). Another section was incubated in a solution containing nitro blue tetrazolium (0.01 g/10 mL distilled water), 0.2 M phosphate buffer pH 7.6, and 0.2 M sodium succinate for 2 h at 37 °C (succinate dehydrogenase) (Sheehan and Hrapchak 1989). Stained sections were viewed under an Olympus BX51 light microscope (Olympus, Tokyo, Japan) at a magnification of 40×. Images were taken using a Olympus DP70 camera. The area and number of muscle fibers were measured in 5 randomly selected fields (approximately 250 fibers in each field) using analysis 5 life science soft image system (Olympus). The diameter of muscle fiber type 1 (βR), type IIA (αR), and type IIB (αW) was calculated. The proportions of muscle fiber types were calculated by dividing the number of each muscle fiber type by the total number of muscle fiber types.

Transmission electron microscopy

Muscle fibers from L. thoracis were dissected and immediately placed in fixative solution (Karnovesky's fixative; 2.5% glutaraldehyde and 4% paraformaldehyde in 1 M cacodylate buffer pH 7.2). Muscle fibers was fragmented under stereomicroscope to small sizes of 1 mm3 using razor blade and placed in a fresh Karnovesky's fixative for 2 h at 4 °C, and then washed twice in 10 mL of 1 M cacodylate buffer. Muscle fibers were fixated in 1% Osmium Tetraoxide in distilled water for 60 min. Further 3 changes of 10 min washes in 1 M cacodylate buffer were carried out to wash off excess Osmium Tetroxide, then samples placed in graded concentration of acetone followed by 3 changes of absolute acetone. The blocks were embedded in pure Araldite epoxy resin and polymerized overnight at 60 °C. Semi-thin section, 0.5 μm was prepared, stained with Toludine blue, and viewed under light microscope for selection of areas of interest. Ultra-thin sections (60 to 90 nm) were cut using a diamond knife and Leica UCT ultra microtome, stained with aqeous urtanyl acetate and lead citrate, and examined with JEOL JEM-1230 transmission electron microscope equipped with a Gatan 792-CCD camera attached to transmission Electron Microscope (JEOL 1230, 120kv) to transfer electrical images into digital images (Gatan, Inc., Pleasanton, Calif., U.S.A.). Electron images of muscle fiber ultrastructures were recorded.

Meat quality evaluation

Meat quality measurements including ultimate pH, expressed juice, cooking loss, shear force, sarcomere length, myofibrillar fragmentation index, and color L*, a*, b* were determined. The ultimate pH was assessed in homogenates at 20 to 22 °C (using an Ultra-Turrax T25 homogeniser; IKA-WERKE GMBH and C.KG JANKE and KUNKEL-STR.10, 79219, Staufen, Germany) of duplicate 1.5 to 2 g of muscle tissue in 10 mL of neutralized 5-mM sodium iodoacetate and the pH of the slurry measured using a Metrohm pH meter (Model Nr 744) with a glass electrode. Chilled muscle samples (13 × 13 mm cross section) for assessment of shear force by a digital Dillon Warner-Bratzler shear machine were prepared from muscle samples cooked in a water bath at 70 °C for 90 min. Sarcomere length by laser diffraction was determined using the procedure described by Cross and others (1980/1981). Myofibrillar fragmentation index was measured using a modification of the method of Johnson and others (1990). This basically measured the proportion of muscle fragments that passed through a 231-μm screen after sample had been subjected to a standard homogenization treatment. A 5 g (±0.5 g) sample of diced (6 mm3 pieces) was added to 50 mL of cold physiological saline (85% NaCl) plus 5 drops of antifoam A emulsion (Sigma-Aldrich Chemical GmbH, Steinheim, Germany) in a 50-mL graduated cylinder, and homogenized at 1/4 speed using an 18-mm dia shaft on an Ultra-Turrax homogenizer for 30-s period. The homogenate was poured into a pre-weighed filter (231 × 231 μm holes). The filter typically ceased dripping after 2 to 3 h, at which time they were dried at 26 to 28 °C in an incubator for 40 h before being re-weighed. The myofibrillar fragmentation index values presented herein were calculated as 100 minus the percentage of the initial meat sample weight that remained on the filter. Expressed juice was assessed by a filter paper method, as the total wetted area less the meat area (cm2) relatively to the weight of the sample (g). Approximately 60 min after exposing the fresh surface, CIE L*, a*, b* light reflectance coordinates of the muscle surface were measured at room temperature (20 ± 2 °C) using minolta Chroma Meter CR-300 (Minolta Co. Ltd., Tokyo, Japan).

Chemical analysis

All visible fats were removed from the muscle samples before they were placed in plastic containers and dried in an Edward freeze dryer (Modulyo) for 5 d under 80-m bar pressures at –60 °C. They were then ground to a homogenous mass in a grinder then used for chemical analyses. The proximate chemical composition of the muscle tissue was determined according to the standard methods of AOAC (2000). Protein was determined using a Foss Tecator Kjeltec 2300 Nitrogen/Protein Analyzer (Foss Teactor AB, Hoganas, Sweden). 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. Evaluation of mineral levels in L. thoracis muscle sample was carried out after complete digestion using a microwave laboratory system type Milestone 1200 MDR, with a maximum temperature of 200 °C in closed polytetrafluoroethylene (PTFE) bombs. An Inductively Coupled Plasma Optical Emission Spectrometer (ICP-OES) type Perkin Elmer Model 3300 (Italy), equipped with a low-flow Gem Cone nebulizer (type of nebulizer designed to handle a range of inductively coupled plasma optical emission spectrometry) in addition to an ultrasonic nebulizer for the detection of very low concentrations was used for mineral analyses. All reagents used were of certified analytical reagent grade and in-house reference materials were used in the analysis. A mixture of concentrated HNO3 and 30% H2O2 was used for the digestion of samples. Calibration graphs were prepared by the addition of known amounts of standard metal solutions to the PTFE bombs and were subjected to the same acid digestion. The digestion procedure consisted of the following steps: 5 mL of concentration HNO3 and 1 mL of 30% H2O2 were added to each digestion bomb. The digestion bombs were placed in the microwave oven. They were then heated from room temperature to 200 °C over a 5-min period, and then held at 200 °C for another 20 min. The digest obtained was collected in 50-mL volumetric flasks, made up to volume and analyzed for a set of minerals by ICP-AES using the manufacturer's recommended conditions.

Statistical analysis

The general liner model (GLM), ANOVA procedure within SAS (1993) was used to compare the effect of electrical stimulation in muscle fiber type, chemical composition, minerals, and meat quality characteristics of L. thoracis muscles in one-humped camel and Omani beef. Significant differences between means were assessed using the least significant difference procedure. Interaction between the electrical stimulation, age, and aging were excluded from the model when not significant (P > 0.05).

Results and Discussion

Kinetics of pH decline

The effects of electrical stimulation on L. thoracis muscle pH of camel and beef at 40 min, 1, 2, 4, 6, 8, 10, 12 h postmortem are shown in Figure 1. Species had no significant effect on the rate of pH decline. However, there were differences in muscle pH between the electrically stimulated and nonstimulated groups within each species at various times postmortem. The greatest pH fall by about 0.12 and 0.15 units, 40 min postmortem resulted from electrically stimulated than nonstimulated carcasses from camel and beef muscles, respectively. Moreover, electrical stimulation led to significantly lower muscle pH values (P < 0.05) during the first 12 h postmortem (Figure 1), as has also been reported for camel and beef (Li and others 2006; Kadim and others 2008c). After a relatively fast fall within the first 2 h in both species, the mean pH values underwent a slow decline until the ultimate pH at 24 h postmortem. These findings are in accordance with those of Kadim and others (2008c) and Li and others (2006) that electrical stimulation led to fast fall pH within the first 3 h postmortem. The average difference in pH decline from 1 to 4 h postmortem between the stimulated and nonstimulated carcasses ranged between 0.11 and 0.18 for camel and 0.15 and 0.17 units for beef. The pH decline was lower for camel L. thoracis sample than cattle, which is in agreement with the finding of Soltanizadeh and others (2008), who measured the pH decline in Semitendinosus in one-humped camel and beef. The amounts of glycolytic enzymes in camel are less than cattle due to its having humps (Immonen and Puolanne 2000), which may be caused slower glycogen degradation and pH decline.

Figure 1—.

Mean changes in pH within the Longissimus thoracis muscle of camel and beef electrical stimulated or nonstimulated (cattle stimulated: - - □ - -, or nonstimulated: - -□- -, camel stimulated: - - - • - - -, nonstimulated: —•—).

Muscle fiber types

Staining of the camel and beef L. thoracis for acid-labile myofibrillar ATPase histochmistry enabled identification of 3 muscle fiber types (Figure 2). The proportions, diameters, and relative area of these fiber types are presented in Table 1. According to the classification of Brooke and Kaiser (1970), the 3 muscle fiber types were named slow twitch Type I, fast-twitch Type IIA, and IIB. The mATPase staining following acidic preincubation (pH 4.35) allowed a distinction between black Type I, unstained Type IIA, and gray Type IIB fibers. The proportion of Type I, IIA, and IIB were 33.1%, 25.2%, and 41.8% in camel and 33.9%, 25.4%, and 40.8% in beef muscles. The contractile type (fast or slow), as indicated by the slow/fast fiber ratio, was similar in both species. Type IIB was significantly (P < 0.05) higher than Type I or Type IIA in both species. Kadim and others (2008c) working with the similar age range of camel ages found that the proportion of Type IIA in L. thoracis muscle was the highest compared to Type I and Type IIB. Kassem and others (2004) also reported that the mean percentages of Type I, Type IIA, and Type IIB fiber types in L. thoracis of 2-y-old camel muscles were 14.5%, 46.7%, and 38.8%, respectively. Differences between the finding of the current study and that of Kassem and others (2004) might be attributed to variations between the camels due to heterogeneity of dromedary camels as there are no improved pure camel breeds as in other species. According to the SDH staining, skeletal muscle fibers were classified as weakly, moderately, or highly oxidative (Figure 2). Whereas all Type I and IIA fibers were highly oxidative, IIB fibers exhibited a heterogeneous SDH staining. Thus, IIB fibers were either weakly or moderately stained in L. thoracis muscle. Muscle fiber diameter and relative area of the muscle fiber types was significantly different between the camels and cattle. The size of muscle fiber types was significantly larger in camels than in beef, which it is most probably related to animal size (141 compared with 304 kg carcass weight for cattle and camel, respectively). Muscle fiber diameter and relative area of the 3 muscle fiber types was significantly (P < 0.05) different between stimulated and nonstimulated L. thoracis samples from both species (Table 2). The difference between stimulated and nonstimulated samples in muscle fiber types from both species may be due to contraction of muscle fibers during the stimulation, as muscle samples were frozen in liquid nitrogen immediately after stimulation. Due to lack of literature reports on camel meat, our conclusions are supported by work on beef meat. In this respect, the presence of contraction bands was reported in muscles from stimulated beef carcasses by Savell and others (1978). The contraction bands were assumed to be formed due to extreme shortening of the sarcomere length. Moreover, Luo and others (2008) have also observed contraction bands in the Longissimus dorsi muscles in electrically stimulated beef carcasses. On the basis of histological evidence, George and others (1980) reported the presence of irregular bands, similar to contraction bands, on muscle fibers from electrically stimulated beef samples.

Figure 3—.

Micrograph from sections of electrically stimulated and nonstimulated sections of camel and cattle Longissimus thoracis muscles (magnification 25000×) showing a region of supercontracture, swollen mitochondria, stretched sarcomere, and pronounced transverse element (muscle fiber bundles distorted and disintegrated and spaces between fibers and disintegration at interfibrillar bridges). The muscle was fixed immediately after electrical stimulation.

Table 1—.  Means and standard error of mean (SEM) for muscle fiber characteristics of Longissimus thoracis muscle from electrical stimulated (ES) and nonstimulated (NS) camel and beef carcasses.
 Species (S)SEMEffectsA
CamelBeef
ESNSESNSSESS×ES
  1. ASignificance: *P < 0.05. Means in the same row with different superscripts are significantly different (P < 0.05).

Number of sample10101212    
Proportion
 Type 133.0  33.134.2 33.5 1.22
 Type IIA25.0  25.325.5 25.2 0.84
 Type IIB42.0  41.640.2 41.3 1.19
Diameter μ
 Type 1 92.1b 96.0b64.9a68.5a2.66*
 Type IIA 99.1b104.7b78.9a83.2a2.63*
 Type IIB103.5ab108.2b95.9a98.0a2.91**
Area
 Type 16811b7410b3402a3820a345*
 Type IIA7833b8831b4964a5513a396*
 Type IIB8628ab9426b7330a7633ab658**
Table 2—.  Means and standard error of mean (SEM) for a range of quality characteristics of electrical stimulated (ES) and nonstimulated (NS) camel and beef Longissimus thoracis muscle.
 Species (S)SEMEffectsA
CamelBeef
ESNSESNS(S)ESS×ES
  1. ASignificance: *P < 0.05. Means in the same row with different superscripts are significantly different.

Number of sample10101212    
Ultimate pH  5.68a  5.79b  5.60a  5.75b0.09*
Expressed juice40.7b35.8a35.4a32.7a1.51***
Cooking loss%32.4b24.3a24.6a23.8a1.55***
Sarcomere length (μm)  1.81c  1.71b  1.75b  1.55a0.13*
Myofibrillar fragmentation index (%)81.9a75.8b78.9a74.9b1.89*
Shear force value (kg)  5.51a  6.83b  5.89a  6.93b0.83*
Color lightness (L*)43.4b39.2a40.2b37.7a1.29*
 Redness (a*)17.1b17.4b15.1a15.7a1.06*
 Yellowness (b*)  6.06a  6.16a  5.62a  5.84a0.44

Meat quality

The ultimate pH of L. thoracis muscles for electrically stimulated and nonstimulated camel and beef carcasses were for 5.68 and 5.79 camel and 5.60 and 5.75 for cattle, respectively (Table 2). The ultimate pH of muscle is a major determinant of meat quality (Watanabe and others 1996) and is related to the rate of glycogen breakdown. Ultimate pH has an important influence on color, expressed juice, and tenderness. The mean ultimate pH of 5.68 (camel) and 5.60 (beef) for the electrically stimulated carcasses L. thoracis samples was significantly (P < 0.05) lower than the 5.79 (camel) and 5.75 (beef) for nonstimulated samples. Dutson and others (1982) stated that meat quality does not improve by electrical stimulation unless it markedly accelerated postmortem glycolysis. In the present study, electrical stimulation consistently produced a more rapid muscle pH decline in both species (Figure 1), which may contribute to enhance quality parameters.

The ultimate pH value of the camel meat was within the range reported for most meat animals (Kadim and Mahgoub 2006; Kadim and others 2006, 2008a,b,c; Shariatmadari and Kadivar 2006). However, in the present study, camel meat had slightly higher mean ultimate pH value (5.74) to those of beef meat (5.68). In contrast, ultimate pH was significantly (P < 0.05) higher (5.90) in camel meat relative to that of Holstein cow (5.63) (Shariatmadari and Kadivar 2006). Similarly, Soltanizadeh and others (2008) found that camel semitendinosus muscle had significantly high pH at 24 h postmortem than beef cattle. The slight difference in ultimate pH between camel and cattle muscles in the present study might have been due to differences in proportions of muscle fiber types or lower muscle glycogen stores at the time of slaughter. Muscle fiber types have different metabolic functions (Ashmore and others 1972). Ashmore (1974) noted that Type IIA fibers have in addition to high metabolic capacity for oxidative metabolism, a capacity for glycogenolytic metabolism, not much lower than that of Type IIB fibers. The present study indicated that the higher proportion of Type IIB related to low ultimate pH. Similar findings were reported by Ozawa and others (2000) with beef L thoracis. Young and Foote (1984) showed that the ultimate pH of the M. splenius of beef was significantly correlated with type IIA fiber composition, which is in line with findings in camel L. thoracis muscles in the present study.

Muscles from camel and beef electrically stimulated carcasses had significantly (P < 0.05) lower shear force value (5.51 and 5.89 kg) compared to non stimulated carcasses (6.83 and 6.93 kg), respectively (Table 2). The main mechanism through which electrical stimulation improves tenderness is assumed to be rapidly decreasing the concentration of adenosine triphosphate and reduces the likelihood of myofibrillar contraction which causes cold shortening (Davey and Gilbert 1974). In the present study, muscles were chilled within 2 to 2.5 h postmortem, therefore, nonstimulated muscles were significantly (P < 0.05) tougher than electrically stimulated samples, suggesting that chilling was the cause of cold shortening. The findings of the present study suggested that electrical stimulation could have caused changes in postmortem camel and beef muscles by either physical disruption of the myofibrillar matrix (Figure 3) or acceleration of proteolysis (MFI: Table 3) (Hwang and others 2003). Histological images showed the appearance of contracture bands predominantly stretched as well as occurrence of ill-defined and disrupted sarcomere (Figure 3). This implies that physical disruption improves tenderness by reducing the resistance to mechanical shearing force. Other studies have also advocated a link between physical disruption and improved tenderness for high (300 to 500 volts) (Will and others 1980; Takahashi and others 1987) and for intermediate voltage (145 to 250 volts) (Sorinmade and others 1982; Ho and others 1996) systems. The value for shear force was not different between camels (6.17 kg) and beef meat (6.41 kg). This study indicated that camel can produce a tender meat, which is comparable to beef, when slaughtered at or below 3 y of age. Similar conclusions were reported by Kadim and others (2006, 2008a). Shariatmadari and Kadivar (2006) also found that the 3-y-old one-humped camel had significantly lower shear force value (5.09) than Holstein cows (6.39). In muscles that are cooled while still a pre-rigor condition, cold shortening might take place. Therefore, the muscles in the present study might have undergone cold shortening, which has been shown to be associated with high shear force and low sarcomere length.

Figure 2—.

Identification of myofibers types by histochemistry and distribution of the different myosin heavy chain in longissimus muscle. Histochemistry demonstration of ATPase after preincubation at pH 4.35 and succinic dehydrogenase activity.

Table 3—.  Means and standard error of mean (SEM) for chemical composition of electrical stimulated (ES) and control camel and beef M. Longissimus thoracis.
 Species (S)SEMEffectsA
CamelBeef
StimulatedNonstimulatedStimulatedNonstimulatedSESS×ES
  1. ASignificance: *P < 0.05. Means in the same row with different superscripts are significantly different.

Number of sample10101212    
Moisture (%)74.8b74.3b68.9a68.5a1.28**
Fat (%)  2.76a  2.79a  7.83b  7.80b0.98**
Protein (%)21.1 21.6 21.8 22.2 0.82
Ash (%) 1.34 1.31 1.47 1.500.04

Low-voltage electrical stimulation tended to increase the CIE L*, a*, and b* values with significantly (P < 0.05) improved muscle lightness (L*) (Table 2). This is in line with the reports of King and others (2004) and Riley and others (1981) who reported that lean from electrically stimulated carcasses have a brighter red color than lean from nonstimulated carcasses. Many factors including myoglobin concentration, ultimate pH, and muscle fiber type, electrical stimulation, and cooling rate influence the development of muscle color (MacDougall and Rhodes 1972; Faustman and Cassens 1990). Postmortem protein degradation is also related to low pH, which increase light scattering properties of meat and thereby increase L*, a*, and b* values (Offer 1991).

Meat from camel muscle was significantly redder (17.4 compared with 15.7 a*) than that of cattle (Table 2). These results are in agreement with those reported for camel and beef (Kadim and others 2008a). Moreover, the color values of the present study for both species were similar in L* values, but relatively higher in a* values and lower in b* values than those reported by Shariatmadari and Kadivar (2006) for Iranian camels and Holstein cattle. The latter researchers found that the camel meat had slightly higher L* (43.2 compared with 39.0), a* (12.7 compared with 11.4), and b* (12.0 compared with 10.3) than cattle meat. This darker color is more likely a result of increased myoglobin content (Lawrie 1979). Other factors that may cause this phenomenon include muscle fiber type differences (Faustman and Cassens 1990; Abril and others 2001). Postmortem protein degradation increases light scattering properties of meat and thereby increases the lightness value (Offer 1991), which is also directly related to the pH (Abril and others 2001). Abril and others (2001) reported that reflectance spectrum value for beef L. thoracis was higher at ultimate pH above 6.1. In the present study, the moderately high pH values might have led to degradation of more protein.

The expressed juice is related to the status of myofibrils, pH, attachment of cross-bridges between thick and thin filaments at the onset of rigor, and denaturation of myosin (Offer and Knight 1988). In the present study, expressed juice significantly differed between electrically stimulated and non-stimulated muscles for the camel meat only (Table 2). Filter paper wetness of camel samples was significantly higher (P < 0.05) for electrically stimulated muscle samples than for non-stimulated ones. The decrease in myofibrillar expressed juice of electrically stimulated muscles may be partly due to the presence of denatured sarcoplasmic proteins in the myofibrillar fraction. Eikelenboom and Smulders (1986) and Den Hertog-Meischke and others (1997) suggested that the decrease in expressed juice of electrically stimulated muscles might be due to increased denaturation of sarcoplasmic proteins. The results of the present study showed that expressed juice was significantly affected by species, with camels having higher express juice than cattle meat samples (38.3 compared with 34.1 mg/cm3) (Table 2). In contrast, Shariatmadari and Kadivar (2006) found no significant difference in expressed juice between camel and cattle Longissimus dorsi muscles. These conflicted reports might be due to variations in myofibrillar protein or muscle fat content (Table 3). Miller and others (1968) found a decrease in the expressed juice as fat levels increase. Expressed juice in the present camel meat was higher than in other camelidaes such as the llama and alpaca L. thoracis probably because of the lower fat content in the dromedary (Cristofanelli and others 2004). Moreover, camels L. thoracis muscle had significantly (P < 0.05) higher cooking loss percent than cattle muscle (Table 2). The decreased binding ability of meat, higher moisture content, and lower degree of marbling may contribute to these variations.

The myofibrillar fragmentation index was significantly (P < 0.05) higher in electrically stimulated than nonstimulated muscles in both species, which would be attributed either to variation in muscle pH (Table 2) or to enhanced protein degradation as reflected in electronic microscopic images (Figure 2). Ho and others (1996) stated that electrical stimulated muscle exhibited faster protein degradation than nonstimulated ones. A strong relationship between physical disruption of the myofibrils and tenderness was reported (Ho and others 1996; Thomson and others 1996; Nagaraj and others 2005). There was small difference in myofibrillar fragmentation index between the 2 species (Table 2). Similarly, Soltanizadeh and others (2008) found no differences in myofibrillar fragmentation index between one-humped camel and beef M. semitendinosus. The small variation in myofibrillar fragmentation index between the 2 species in the present study may be due to difference in the enzyme content or the enzyme/inhibitor ratio due to muscle account, which reflect the efficiency of the proteolytic systems (Caballero and others 2007).

Chemical composition

Generally the values for chemical composition were within the reported range for camel meat (Pérez and others 2000; Cristofanelli and others 2004; Kadim and Mahgoub 2006; Kadim and others 2006, 2008a,b,c) and cattle meat (USDA 1986; Mills and others 1992) (Table 3). However, the present study showed that the camel meat contained slightly lower protein and ash levels than the Omani cattle meat. In agreement with the present finding, Elgasim and Alkanhal (1992) reported that camel meat has slightly less protein content than cattle. Naser and others (1965) reported that meat of less than 5-y-old camels contained similar protein to meat of steers. In contrast, Babiker and Tibin (1986) found that camel meat has significantly (P < 0.05) greater total protein than cattle. Nevertheless, camel meat appears to be a good potential source of high-quality protein in harsh climatic arid regions. Moisture is important as far as its pronounced effects on meat shelf life, processing potential, and sensory characteristics. The current study showed that camel meat had significantly (P < 0.01) higher moisture content than cattle sample.

Fat content of L. thoracis muscle in the Omani cattle (7.8%) was significantly (P < 0.01) higher than camel meat (2.8%). In agreement with the current study, Finke (2005) compared cattle and camel meat and found that camel meat contains lower fat. In contrast, Hammam and others (1962) reported that camel Longissimus muscle is fatter, dryer, and lower protein contents than cattle. The lower range of fat content of the current study confirmed that camel meat could be much leaner than cattle meat, especially if it is slaughtered at a younger age. These results support the potential concept that the camel meat is healthier than other red meats (Kadim and others 2008b). Similarly, Elgasim and Alkanhal (1992) reported that camel meat has a fat content of 2.6%, which was lower than that of cattle (4.7%). The moisture-to-protein ratio is a reflection of the suitability of meat for processing (Forrest and others 1975). The similarity in moisture-to-protein ration between the 2 species in the present study (3.31 compared with 3.27) led to an opportunely for processing camel meat. Camel meat in the present study had a slightly less ash content (1.3%) than that of cattle (1.5%), which is in agreement with reports of Elgasim and Alkanhal (1992) of 0.9% and 1.5% ash for camel and cattle meat, respectively.

Levels of macro- and micro-elements (Table 4) for the camel and Omani cattle meats are within the range reported for camel (Kadim and others 2008b) and cattle (USDA 1986; Kadim and others 2008a). They also indicate that camel meat is comparable in mineral composition to cattle except for potassium content. Camel and cattle meat like other red meats contained significantly higher levels of potassium (Greenfield and others 1987a,b; Elgasim and Alkanhal 1992). Cattle had significantly (P < 0.01) higher potassium (1329 compared with 761 mg/kg), magnesium (65.5 compared with 50.9 mg/kg), and phosphorus (517 compared with 414) than camel samples. Potassium was the most abundant element followed by phosphorus, sodium, magnesium, and calcium, respectively. Similar findings were reported by Elgasim and Alkanhal (1992), Dawood and Alkanhal (1995), El-Faer and others (1991), and Kadim and others (2006, 2008b) for one-humped camel.

Table 4—.  Means and standard error of mean (SEM) for macro- and micro-elements of electrical stimulated (ES) and nonstimulated (NS) camel and beef M. Longissimus thoracis.
 Species (S)SEMEffectsA
CamelBeef
ESNSESNSSESS×ES
  1. ASignificance: *P < 0.05, **P < 0.01. Means in the same row with different superscripts are significantly different.

Number of sample10101212    
Calcium (Ca)22.9  23.9  20.0  19.4  8.36  
Magnesium (Mg)50.8a  51.0a  64.9b  66.1b  4.24  *
Sodium (Na)175b181b159a166a15.5   *
Potassium (K)759a762a1331b1326b66**
Phosphorus (P)411a417a512b522b36*
Cadmium (Cd)0.010.010.010.010.002
Chromium (Cr)0.030.030.030.030.002
Nickel (Ni)0.100.100.140.150.014
Lead (Pb)0.060.070.020.020.009
Cobalt (Co)0.010.010.010.010.009
Molybdenum (Mo)0.030.040.020.020.004
Beryllium (Be)0.010.010.020.020.002
Vanadium (V)0.020.020.020.020.002

Conclusions

Electrical stimulation had significant effects on meat quality characteristics of camel and cattle M. Longissimus thoracis including pH, expressed juice, shear force value, sarcomere length, MFI, and color. These effects were mostly due to ultrstructural alterations as well as enhanced protein degradation. Camel meat is comparable to cattle meat in nutritive value, meat quality, and composition, when slaughtered at comparable age range. Camel would have an edge over cattle due to its low intramuscular fat content. In view of the findings of present study, low-voltage electrical stimulation can be used to improve camel meat quality characteristics.

Acknowledgments

The authors express their gratitude to the staff of the Dept. of Animal and Veterinary Sciences for their technical assistance with quality and composition measurements.

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