Meat Science 82 (2009) 77–85

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Meat Science

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Effect of low voltage electrical stimulation on biochemical and qualitycharacteristics of Longissimus thoracis muscle from one-humped Camel(Camelus dromedaries)

I.T. Kadim a,*, Y. Al-Hosni a, O. Mahgoub a, W. Al-Marzooqi a, S.K. Khalaf a, R.S. Al-Maqbaly a,S.S.H. Al-Sinawi b, I.S. Al-Amri b

a Department of Animal and Veterinary Sciences, College of Agricultural and Marine Sciences, Sultan Qaboos University, Muscat, Omanb Department of Pathology, College of Medicine and Health Sciences, Sultan Qaboos University, P.O. Box 34, Al-Khoud 123, Muscat, Oman

a r t i c l e i n f o

Article history:Received 14 April 2008Received in revised form 10 December 2008Accepted 11 December 2008

Keywords:CamelLongissimus thoracisElectrical stimulationWB-shear forceMuscle fibre typeMyofibrillar fragmentation index

0309-1740/$ - see front matter � 2009 Elsevier Ltd. Adoi:10.1016/j.meatsci.2008.12.006

* Corresponding author. Tel.: +968 99279776; fax:E-mail address: isam@squ.edu.om (I.T. Kadim).

a b s t r a c t

The effects of electrical stimulation (90 V) 20 min post mortem on meat quality and muscle fibre types offour age group camels (1–3, 4–6, 7–9, 10–12 years) camels were assessed. Quality of the Longissimus tho-racis at 1 and 7 days post mortem ageing was evaluated using shear force, pH, sarcomere length, myofibr-illar fragmentation index, expressed juice, cooking loss and L*, a*, b* colour values. Age of camel andelectrical stimulation had a significant effect on meat quality of L. thoracis. Electrical stimulation resultedin a significantly (P < 0.05) more rapid pH fall in muscle during the first 24 h after slaughter. Muscles fromelectrically-stimulated carcasses had significantly (P < 0.05) lower pH values, longer sarcomeres, lowershear force value, higher expressed juice and myofibrillar fragmentation index than those from non-stim-ulated ones. Electrically-stimulated meat was significantly (P < 0.05) lighter in colour than non-stimu-lated based on L* value. Muscles of 1–3 year camels had a significantly (P < 0.05) lower shear forcevalue, and pH, but longer sarcomere, and higher myofibrillar fragmentation index, expressed juice, andlightness colour (L*) than those of the 10–12 years camels. The proportions of Type I, Type IIA and TypeIIB were 25.0, 41.1 and 33.6%, respectively were found in camel meat. Muscle samples from 1–3 yearcamels had significantly (P < 0.05) higher Type I and lower Type IIB fibres compared to those from 10–12 year camel samples. These results indicated that age and ES had a significant effect on camel meatquality.

� 2009 Elsevier Ltd. All rights reserved.

1. Introduction

The one-humped camel (Camelus dromedaries) is the most use-ful domestic animal specie for animal production in the arid andsemi arid regions. They can produce good quality meat at compar-atively low cost under extremely harsh environments. The camelhas great tolerance to high temperatures, solar radiation, waterscarcity, sandy terrain and poor vegetation due to their uniqueanatomy and physiology as well as for their feeding habits (Sha-lash, 1983). The camel, therefore, can be economically raised formeat production in these ecologically constrained areas (Tandon,Bissa, & Khanna, 1988).

A camel carcass can provide a substantial amount of meat forhuman consumption. There is evidence of a great demand for freshcamel meat and for camel meat in blended meat products even insocieties not herding camels (Morton, 1984; Pérez et al., 2000; Sha-lash, 1979). This demand for camel meat appears to be increasing

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+968 24413418.

due to health reasons. Camel meat contains less fat, lower choles-terol and relatively high polyunsaturated fatty acids compared tobeef (Dawood & Alkanhal, 1995; Kadim, Mahgoub, & Purchas,2008; Rawdah, El-Faer, & Koreish, 1994). These characteristicsare important for reducing cardiovascular diseases risk related tohigh saturated fat consumption (Giese, 1992). As camels are gener-ally used in less developed countries, research into improving meatcharacteristics is lacking (Skidmore, 2005). There is also reluctancetowards consuming camel meat in general as it is thought to betough, coarse and watery. This is mainly because camel meat usu-ally comes from old animals that have served other functions intheir life or predominantly at the time their labour performanceand milk yield declines (Wilson, 1998). However, many investiga-tors reported that quality characteristics of the camel meat arevery similar to that of beef if they are slaughtered at a comparableage (Elqasim, Elhag, & Elnawawi, 1987; Kadim et al., 2008; Tandonet al., 1988).

An approval to increase post mortem muscle metabolism andhasten the onset of rigor mortis might improve the quality charac-teristics of camel meat. Additionally, a more rapid pH decline could

78 I.T. Kadim et al. / Meat Science 82 (2009) 77–85

potentially result in a brighter coloured meat (King et al., 2004; Ri-ley, Savell, Smith, & Shelton, 1981). Electrical stimulation is a pro-ven method for improving tenderness and meat colour fromseveral species (McKeith, Savell, Smith, Dutson, & Shelton, 1979;Savell, Smith, Dutson, Carpenter, & Suter, 1977). No reports areavailable on the effects of electrical stimulation on meat qualitycharacteristics of camel meat. The objectives of the present studywere to investigate the effect of age (1–3, 4–6, 7–10 and 10–12years), ageing (1 vs. 7 days) and low voltage electrical stimulationon biochemical changes and meat quality characteristics of theLongissimus thoracis muscle of the one-humped Omani camel.

2. Materials and methods

2.1. Animals

A total of 72 Arabian one-humped camels representing four agegroups: Group 1 (1–3 years old: n = 16), Group 2 (4–6 years old:n = 16), Group 3 (7–10 years old: n = 16) and Group 4 (10–12 yearsold: n = 24) were sampled. The animals were exposed to normalpre-slaughter handling and transportation processes and subse-quently held in a lairage for 1–2 h. Animals were slaughtered anddressed following routine commercial slaughterhouse proceduresaccording to Halal methods. The ambient temperatures on slaugh-ter days ranged between 25 �C and 27 �C.

2.2. Electrical stimulation

Fifty percentage of the carcasses within each age group wererandomly selected and subjected to electrical stimulation using aV1.3-R3B stimulator (7.5 ms duration every 70 ms (14 Hz) and anoutput of 90 V, AgResearch, New Zealand). During electrical stimu-lation the carcasses were suspended on a gambrel by a hook. Car-casses were stimulated with a battery clip attached to the neck andstainless steel hook contacting the Achilles tendon. The currentwas applied for 60 s, 20 min after complete bleeding.

2.3. Muscle samples

The L. thoracis muscle of the left and right sides were removedbetween the 10–13 ribs (800–1000 g) of each of the camel carcasswithin 20 min post slaughter. Samples were kept in zipped plasticbags in an insulated box, then transferred to a chiller (1–3 �C) with-in about 4–4.5 h post mortem and kept for 24 h before runningquality measurements. The samples from the left side of each car-cass were then frozen (24 h post mortem), while the samples fromthe right side were kept in the chiller (2–3 �C) for another six days(seven days ageing) and then frozen.

2.4. Muscle pH decline

The pH for the L. thoracis muscles from each side were moni-tored using a portable pH meter (Hanna waterproof pH meter,Model Hi 9025) fitted with a polypropylene spear-type gel elec-trode (Hanna Hi 1230) and a temperature adjusting probe. Mea-surements, designated as pH (40 min, 1, 2, 4, 6, 8, 10, 12, 24 hrpost mortem) were recorded. For each measurement, the pH probeand the thermometer were inserted into muscles to a similardepth.

2.5. Histochemistry

Core samples of the right L. thoracis at the last rib location wereremoved immediately after electrical stimulation cut into 1 � 1 cmpieces (parallel to the muscle fibres) and frozen in iso-pentane

cooled in liquid nitrogen and then snapped in liquid nitrogen. Sam-ples were stored at �80 �C Ultra-Low Temperature Freezer (MDF-392, Sanyo Electric Biomedical Co. Ltd. Japan) until further analysis.Muscle samples were cut into 8-lm-thickness on a cryostat (ModelBright, England) at �23 �C, and mounted on silane-treated micro-scope slides. Two sections from each sample were incubated inan acid at pH 4.35 and 4.60 for 10 min and then incubated atATP substrate (adenosine 5-triphosphate) pH 9.5 for 45 min. Thesections were then incubated for three minutes in an aqueous co-balt chloride and finally, they were incubated in a solution ofammonium sulphide. A blackish–brownish cobalt sulphide is gen-erated in the reaction to replace cobalt phosphate (Brooke & Kaiser,1970). One more section from each sample was stained for succi-nate dehydrogenase; the section was incubated in a solution con-taining nitro blue tetrazolium, 0.2 M phosphate buffer pH 7.6 and0.2 M sodium succinate for two hours at 37 �C. The dehydrogenaseenzyme in the muscle section act on the substrate and the tetrazo-lium salt is reduced to from blue-purple deposition at the site ofthe enzyme activity. (Sheehan & Hrapchak, 1989). Staining sectionswere viewed under a Leitz (Wetzlar, Germany) divert invertedphase contrast-fluorescence microscope at a magnification of160{. Images were taken using a Spot 2 Slider (model 1.4.0, Diag-nostic Instruments, Inc.) camera. The cross-sectional area of 500 fi-bres on four viewing frames per sample was measured using IP Labscientific imaging software (Scanalytics, Inc., Fairfax, VA). Thediameter for each muscle fibre type was calculated. The propor-tions of muscle fibre types were calculated by dividing the numberof each muscle fibre type by the total number of muscle fibre typesin an area containing at least 1500 fibres.

2.6. Transmission electron microscopy

L. thoracis fresh muscle fibres were dissected and placed imme-diately after the electrical stimulation in vials containing electronmicrocopy fixative solution (Karnovesky’s fixative; 2.5% gluteral-dehyde and 4% paraformaldehyde in 1 M cacodylate buffer pH7.2). Muscle biopsies was fragmented under stereomicroscope tosmall sizes of 1 mm3 using razor blade and placed in a fresh Karno-vesky’s fixative for 2 h at 4 �C, and then washed in three 10 minchanges of 1 M cacodylate buffer. The remaining processing stepswere carried out by Leica automatic tissue processor. Secondaryfixation was carried out in 1% Osmium Tetraoxide in distilled waterfor 60 min. Further three changes of 10 min washes in 1 M cacodyl-ate buffer were carried out to wash off excess Osmium Tetroxide,then samples were placed in graded concentration of acetone fol-lowed by three changes of absolute acetone. The blocks were theninfiltrated with Araldite epoxy resin. Embedded in pure Aralditeepoxy resin and polymerized overnight at 60 �C. Semi-thin section,0.5 lm was prepared, stained with Toludine blue and viewed un-der light microscope for selection of section areas of interest. Ultrathin sections (60–90 nm) were cut using a diamond knife and leicaUCT ultra microtome, stained with aqeous urtanyl acetate and leadcitrate and examined with JEOL JEM-1230 transmission electronmicroscope equipped with Gata 792-CCD camera operated at60 kV. Electron images of muscle fibre ultrastructures recorded.

2.7. Meat quality evaluation

The L. thoracis muscles were evaluated for a range of qualitycharacteristics including ultimate pH, expressed juice, cookingloss%, Warner-Bratzler shear force value, sarcomere length, myo-fibrillar fragmentation index and colour (L*, a*, b*). The ultimatepH was assessed in homogenates at 20–22 �C (using a Ultra TurraxT25 homogenizer) of duplicate 1.5–2 g of muscle tissue in 10 ml ofneutralized 5-mM sodium iodoacetate and the pH of the slurrymeasured using a Metrohm pH meter (Model No. 744) with a glass

5.8

6

6.2

6.4

6.6

pH v

alue

I.T. Kadim et al. / Meat Science 82 (2009) 77–85 79

electrode. Chilled muscle samples (13 mm � 13 mm cross section)for the assessment of shear force by a digital Dillon Warner-Brat-zler shear machine were prepared from muscle samples cookedin a water bath at 70 �C (±0.5 �C) for 90 min. sarcomere length bylaser diffraction was determined using a procedure described byCross, West, and Dutson (1980/1981). Express juice was assessedby a filter paper method, as the total wetted area less the meat area(cm2) relatively to the weight of the sample (g). Approximately60 min after exposing the fresh surface, CIE L*, a*, b* light reflec-tance coordinates of the muscle surface were measured at roomtemperature (25 ± 2 �C) using a Minolta Chroma Meter CR-300(Minolta Co., Ltd., Japan), with a colour measuring area 1.1 cmdiameter. Myofibrillar fragmentation index was measured using amodification of the method of Johnson, Calkins, Huffman, Johnson,and Hargrove (1990). This measured the proportion of muscle frag-ments that passed through a 231-lm filter after the sample hadbeen subjected to a standard homogenization treatment. A 5 g(±0.5 g) samples of diced muscle (6 mm3 pieces) was added to50 ml of cold physiological saline (85% NaCl) plus five drops ofantifoam A emulsion (Sigma Chemical A5758) in a 50 ml graduatedcylinder, and homogenized at 1=4 speed using an 18 mm diametershaft on an Ultra-Turrax homogenizer for 30-second periods sepa-rated by a 30 s rest period. The homogenate was poured into aweighed filter (231 � 231 lm holes). The filter typically ceaseddripping after 2–3 h, at which time they were dried at 26–28 �Cin an incubator for 40 h before being reweighed. The myofibrillarfragmentation index values presented herein were calculated as100 minus the percentage of the initial meat sample weight thatremained on the filter.

5.60 1 2 3 4 5 6 7 8 9 10 11 12

Time (hours)

Fig. 1. Mean changes in pH within the Longissimus thoracis muscle in carcasses fromfour age groups (group 1: 1–3 years, group 2: 4–6 years, group 3: 7–9 years andgroup 4: 10–12 years) of Arabian camel, which was electrically-stimulated or non-stimulated (1–3 years: electrically-stimulated: --h- -, or non-stimulated: –h–, 4–6years: electrically-stimulated: --d--, non-stimulated: –d–, 7–9 years: electrically-stimulated: --N- -, or non-stimulated: –N–, 10–12 years: electrically-stimulated: --j--, or non-stimulated –j–).

2.8. Statistical analysis

The effect of low voltage electrical stimulation (electrically-stimulated vs. non-stimulated), age (1–3, 4–6, 7–9 and 10–12years) of camel and ageing (one vs. seven days) of L. thoracis mus-cle samples on muscle fibre types and meat quality and theirinteraction were analyzed using analysis of variance procedure(SAS, 1993). Significances between means were assessed usingthe least-significant-difference procedure. Interaction betweenthe electrical stimulation, age and ageing were excluded from themodel when not significant (P > 0.05).

3. Results and discussion

3.1. Kinetics of pH decline

Effects of electrical stimulation on L. thoracis muscle pH withinthe four age groups of the camel at 40 min then hourly between 2and 12 h post mortem are given in Fig. 1. Although, the age had nosignificant effect on the rate of pH decline, there were significant(P < 0.05) differences in muscle pH between the electrically-stimu-lated and non-stimulated groups within each age group at varioustimes post mortem. The most readily measurable effect of electri-cal stimulation was the rapid drop in pH, which regarded as anindicator of effectiveness of stimulation. In the present study, thegreatest pH fall occurred at 40 min post mortem resulting fromelectrical stimulation applied 20 min after slaughter. It is particu-larly interesting to note that low voltage electrical stimulation ap-plied at 20 min, dropped significantly (P < 0.05) the pH by about0.14 units below the non-stimulated group. This effect with electri-cal stimulation applied as late as 20 min, after slaughter, was unex-pected in view of other reports (Bendall, 1980; Fabiansson,Jonhsson, & Ruderus, 1979), which indicated that low voltage stim-ulation were effective only if applied within a few minutes ofslaughter. Moreover, electrical stimulation led to significantly low-

er muscle pH values (P < 0.05) during the first 12 h post mortem(Fig. 1), as has been reported for other species (Kadim, Purchas, Da-vies, Rae, & Barton, 1993; Maribo, Ertbjerg, Anderson, Barton-Gade,& Moller, 1999; Wiklund, Stevenson-Barry, Duncan, & Littlejohn,2001; Li et al., 2006). After a relatively fast fall within the first4 h, the mean pH values underwent a slow decline until an ulti-mate pH at 24 h post mortem. These findings are in accordancewith those of Li et al. (2006) that electrical stimulation led to a fastfall in pH within the first 3 h in beef cattle. The average differencein pH (1–4 h post mortem) between the electrically-stimulatedand non-stimulated carcasses ranged between 0.12 and 0.15 units.However, the difference in pH between electrically-stimulated andnon-stimulated carcasses decreased with time as the differencewas 0.15 units at 4 h and 0.08 units at 24 h post mortem.

The overall rate of pH decline variation in camel carcasses be-tween the two treatments was the highest in the 10–12 year Group(0.21 units) and the lowest in the 1–3 year Group (0.06 units). Var-iation in pH among the four age group muscles might be attributedto the difference in proportions of red and white muscle fibre types(Table 3) and, consequently to differences in patterns of energymetabolism during both ante- and post mortem (Swatland,1982). The effect of electrical stimulation is reported to be depen-dent on fibre type; muscles with a higher percentage ofslow-twitch-oxidative fibres responding less intensively to electri-cal stimulation than muscles with a higher percentage of

Tabl

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80 I.T. Kadim et al. / Meat Science 82 (2009) 77–85

fast-twitch-oxidative glycolytic or fast-twitch-glycolytic fibres(Devine, Ellery, & Averill, 1984). This may explain the results ofthe present study, because the percentage of Type IIB was higherin L. thoracis of the older camels than younger ones.

3.2. Ultimate pH

The ultimate pH of L. thoracis muscles varied between 5.53 and5.82 and between 5.60 and 5.86 for electrically-stimulated andnon-stimulated carcasses, respectively (Tables 1 and 2). The ulti-mate pH of a muscle is a major determinant of meat quality(Watanabe, Daly, & Devine, 1996) and is related to the rate of gly-cogen breakdown and liberation of lactate pre- and post mortem.Ultimate pH has an important influence on colour, water-holdingcapacity and tenderness. The ultimate pH value of meat is the re-sult of combination of many factors including pre-slaughter han-dling, post mortem treatment and muscle physiology (Thompson,2002). The most important feature in this study was the significant(P < 0.05) effect of electrical stimulation on ultimate pH. The meanultimate pH of 5.69 for the electrically-stimulated carcasses sam-ples was significantly (P < 0.05) lower than the 5.74 for non-stim-ulated samples. Similar findings have been reported by Bouton,Ford, Harris, and Shaw (1978) and Geesink, Mareko, Morton, andBickerstaffe (2001). It has been reported from bovine studies thatthe ultimate pH might not be reached until 48 h postmortem butthere are no similar reports in camels. Therefore, the differencesin ultimate pH between the electrically-stimulated and non-stim-ulated muscles may also be explained by that at 24 h post mortem,rigor mortis of non-stimulated samples were not complete (Fig. 1).Dutson, Savell, and Smith (1982) emphasized that improvement inmeat quality does not result from electrical stimulation unless itmarkedly accelerated post mortem glycolysis. In the present study,electrical stimulation consistently produced a more rapid glycoly-sis in muscle samples from the four age groups evaluated (Fig. 1).Ashmore et al. (1973) reported that low muscle glycogen stores atslaughter do not allow the development of a desirable pH (approx-imately 5.5) of the lean tissue after slaughter.

Ageing is the process that causes an increase in tenderness overtime and involves specific degradation of structural proteins(Hwang, Devine, & Hopkins, 2003). This resembles the methodadopted in the current study where meat was under temperatureof 2–3 �C for seven days. In the present study, storage L. thoracismuscle for 7 days had no significant effect on ultimate pH valuesof either electrically-stimulated or non-stimulated L. thoracis mus-cles (5.72 vs. 5.71 for 1 and 7 days, respectively). Petersen andBlackmore (1982) suggested that the increased muscle activity inelectrically-stimulated carcass is probably responsible for the morerapid post mortem pH decline. On the other hand, our finding agreewith those of Vergara and Gallego (2000) who observed that inelectrically-stimulated carcasses, pH decreases more rapidly, andageing starts earlier.

The muscles of 10–12 years camels had significantly lower(P < 0.05) pH (5.57) than those of 1–3 years (5.83), 4–6 years(5.71), and 7–9 years (5.70) animals. The middle aged camels (4–6 and 7–9 years groups) had significantly lower ultimate pH valuethan either 1–3 or 10–12 years camels. Similar values for camels ofvarious ages were reported by Kadim and Mahgoub (2007), Kadimet al. (2006, 2008). Generally, young camels tend to produce meatwith a higher pH than older camels, most likely due to low glyco-gen stores in muscle. The low muscle glycogen stores at slaughterdo not allow the development of a desirable pH of the muscle afterslaughter (Ashmore et al., 1973). The trend of high ultimate pH ofthe samples from younger camels in the present study might bedue to differences in proportions of muscle fibre types (Table 3)as well as lower muscle glycogen stores at the time of slaughter.Fibre types have been shown to differentiate at various stages of

Table 3Mean and Standard Error of Mean (SEM) for muscle fibre characteristics ofLongissimus thoracis muscle from four age groups of camels.

Age (year) SEM

1–3 4–6 7–9 10–12

Proportion (%)Type 1 29.94c 26.76bc 24.28b 20.32a 1.517Type IIA 40.13a 40.55ab 39.93b 43.60c 2.001Type IIB 29.93a 32.69ab 35.79bc 36.08c 2.056

Diameter (lm)Type 1 79.44a 96.54b 98.24b 98.37b 4.336Type IIA 90.42a 103.99b 103.27b 108.80b 4.678Type IIB 92.48a 104.28b 108.91b 113.80b 5.200

Area (lm2)Type 1 5252a 7049b 7648b 7786b 609Type IIA 6678a 8620ab 8459ab 9428b 756Type IIB 6951a 8636b 9542b 10332b 911

a,bMeans within the same row with different superscripts were significantly dif-ferent (P < 0.05).

Table 2Effect of age, electrical stimulation, ageing and their interaction on a range of Longissimus thoracis quality characteristics.

Significancea

Age ES Ageing Age � ES Age � Ageing ES � Ageing Age � ES � Ageing

Ultimate pH NS ** NS NS NS NS NSExpressed juice (cm2/g) * * NS NS NS NS NSCooking loss% * ** ** NS NS * NSWB-shear force value (kg) *** *** *** *** *** *** ***

Sarcomere length (lm) * * NS NS NS NS NSMyofibrillar fragmentation index ** * NS NS NS NS NSL* (lightness) NS * NS NS NS NS NSa* (redness) NS NS NS NS NS NS NSb* (yellowness) * NS NS NS NS NS NS

a NS, not significant.* P < 0.05.** P < 0.01.*** P < 0.001.

I.T. Kadim et al. / Meat Science 82 (2009) 77–85 81

animal development and therefore have different metabolic func-tions in the body (Ashmore, Tompkins, & Doerr, 1972). In the pres-ent study, variation in muscle fibre types between the age groupscontributed in differences in patterns of muscle metabolism (Swat-land, 1982), and consequently differences in ultimate muscle pH.Ashmore (1974) noted that Type IIA fibres have in addition to highmetabolic capacity for oxidative metabolism, a capacity for glyco-genolytic metabolism similar to Type IIB fibres. The present studyfound that the higher proportion of Type IIB was related to lowultimate pH. Similar findings were reported by Ozawa et al.(2000) with beef L. thoracis. Young and Foote (1984) showed thatthe ultimate pH of the Musculus splenius of beef was significantlycorrelated with the type IIA fibre composition, which is in line withfindings in camel L. thoracis muscles in the present study.

3.3. Expressed juice

Expressed juice is an important meat quality characteristic be-cause of its influences on the nutritional value, appearance and pal-atability of meat. Drip loss is supposed to be a result of shrinkage ofthe myofibrils due to pH fall post mortem, attachment of cross-bridges between thick and thin filaments at the onset of rigor,and denaturation of myosin (Offer & Knight, 1988). In the presentstudy, ultimate pH differs significantly between electrically-stimu-lated and non-stimulated muscles (Tables 1 and 2). Expressed juicewas significantly higher (P < 0.05) for electrically-stimulated mus-cle samples than for non-stimulated ones. Den Hertog-Meischke,Smulders, Van Logtestijin, and Van Kanapen (1997) and Eikelen-boom and Smulders (1986) suggested that the decrease in water-holding capacity of electrically-stimulated muscles might be dueto an increase in the denaturation of sarcoplasmic proteins. Thelower myofibrillar water-holding capacity of electrically-stimu-lated muscles was most probably not due to differences in pH ofthe myofibrillar protein suspensions (Offer & Knight, 1988). Inthe present study, ageing did not affect the expressed juice of thefour age groups.

In the present study, expressed juice was significantly affectedby age, with 1–3 year-old camels having higher express juice than10–12 year-old animals (Tables 1 and 2), while the value for themiddle age groups of camels was in between. Similarly, Kadimand Mahgoub (2007) and Kadim et al. (2006) found that camelsyounger than 3 years old had significantly higher expressed juicethan the 6 year-old one-humped camels. These differences weredue to variations in fat content or in ultimate pH. Miller, Staffle,and Zirkle (1968) found a decrease in the water-holding capacityas fat levels increase. In agreement with the present study, Dawood(1995) reported that 8 month-old camel meat had significantly(P < 0.05) higher expressed juice than 26 month-old camel meat.

The current study indicated that expressed juice in the camel meatis higher than in other camelidaes such as the llama and alpacaprobably because of the lower fat content in the dromedary (Cris-tofaneli, Antonini, Torres, Polidori, & Renieri, 2004; Kadim et al.,2008). Meat of a high pH value has a greater water-holding capac-ity than low pH value (Abril et al., 2001; MacDougall, 1982).Although electrical stimulation had a negative effect on expressedjuice, cooking loss% was not significantly affected by electricalstimulation (Tables 1 and 2). Cooking loss% was significantly(P < 0.05) lower in 10–12 year camels than in the 1–3 and 4–6 yearcamels. The decreased binding ability of less mature animal meat,higher moisture content and lower degree of marbling may con-tribute to the variations. Similarly, Dawood (1995) found that cam-els at 8 months of age had significantly higher cooking loss% thancamels at 26 month of age.

3.4. Shear force value

Muscles from electrically-stimulated carcasses had a signifi-cantly (P < 0.05) lower shear force value (6.97 kg/cm2) comparedto non-stimulated carcasses (9.47 kg/cm2) (Tables 1 and 2). Themain mechanism through which electrical stimulation improvestenderness is by rapidly decreasing the concentration of adenosinetriphosphate (ATP) this reducing the likelihood of myofibrillar con-traction and cold shortening (Davey & Gilbert, 1974). In the presentstudy, L. thoracis muscles were chilled while still at pre-rigor mor-tis, therefore, non-stimulated muscles were significantly tougher

Fig. 2. Photomicrograph of serial sections of camel Longissimus thoracis muscle,staining for the ATPase, note the activity of the slow myosin isoenzyme of type Ifibres, Type IIB fibres stain more intensely than Type IIA fibres in this species (A),confirmed by staining for succinic dehydrogenase activity, an enzyme associatedwith oxidative phosphorylation (B).

82 I.T. Kadim et al. / Meat Science 82 (2009) 77–85

than electrically-stimulated samples, suggesting that chillingtreatments had induced a degree of cold-shortening. This view isconsidered by the fact that the shear force value of non-stimulatedsamples did not significantly improve with ageing, unlike the elec-trically-stimulated samples. As a consequence, electrical stimula-tion and ageing treatments produced meat which was tendererthan the non-stimulated meat without ageing. The findings ofthe present study indicated that electrical stimulation could exertchanges in post mortem camel muscles by either physical disrup-tion of the myofibrillar matrix (Fig. 3) or by acceleration of prote-olysis (myofibrillar fragmentation index: Table 1) (Hwang et al.,2003). Histological images showed contracture bands predomi-nantly stretched as well as ill-defined and disrupted sarcomeres(Fig. 3: samples were taken immediately after stimulation). Thisimplies that physical disruption lowers the resistance to mechani-cal shearing force. Similarly, other studies have indicated a link be-tween physical disruption and improved tenderness for high (300–500 V) (Takahashi, Wang, Lochner, & Marsh, 1987; Will, Ownby, &Henrickson, 1980) and for intermediate voltage electrical stimula-tion (145–250 V) (Ho, Stromer, & Robson, 1996; Sorinmade, Cross,Ono, & Wergin, 1982).

The most marked differences in meat quality between the fourage groups were in shear force values. The value for shear forcewas significantly (P < 0.05) higher for 10–12 year-old camels

(10.63 kg/cm2) than for either 1–3 year-old (6.27 kg/cm2), 4–6year-old (7.60 kg/cm2), or 7–9 year-old (838 kg/cm2) camels. It iscommonly accepted that younger animals yield more tender meatthan older ones. A number of studies have confirmed the findingsthat shear values increase with increase age of the animals (Asghar& Pearson, 1980; Miller, Cross, & Crouse, 1987; Kadim et al., 2006,2008; Purchas, Hartley, Yan, & Grant,1997). Any differences due toage may be related to histological changes that make place in mus-cle structure and composition as animals mature, particularly inthe connective tissue (Asghar & Pearson, 1980). The high fragmen-tation index in young camel may be caused by easily breakingmyofibrils into shorter segments. The strength of the differentmuscle fibre types had a significant effect on the mechanical prop-erties of the individual fibre types (Christensen, Kok, & Ertbjerg,2006). The variations in muscle fibre types between the four agegroups in the present study were caused shear force variations be-tween the age groups in the present study.

3.5. Myofibrillar fragmentation index

Measurement of myofibril fragmentation is used to determinepost mortem proteolysis in beef, pork, chicken and lamb (Lame-tsch, Knudsen, Ertbjerg, Oksbjerg, & Therkildsen, 2007; Olson, Par-rish, & Stromer, 1976). The myofibrillar fragmentation index wassignificantly (P < 0.05) higher in the electrically-stimulated thanthe non-stimulated muscles, which may be attributed to eithervariation in muscle pH (Tables 1 and 2) or to protein degradationas reflected in electronic microscopic images (Fig. 3). Accordingto Ho et al. (1996), electrically-stimulated muscles exhibited fasterprotein degradation. The present study did not examine a quanti-tative relationship between physical disruption and enhancedendogenous proteolytic activity. However, there is potentially astrong relationship between physical disruption of the myofibrillarcomplex and increase in tenderness (Ho et al., 1996). The differ-ences in rates of fragmentation of myofibrillar proteins may there-fore, account for differences in the rate of post mortemtenderization of meat (Nagaraj, Anilakumar, & Santhanam 2005;Thomson, Dobbie, Singh, & Speck, 1996). Claeys, Uytterhaegen,Demeyer, and De Smet (1994) reported that at higher pH proteinspreferentially solubilized were titin, filamin, neubulin and myosinheavy chain. Except for myosin, all are preferentially degraded bycalpains (Goll, Otsuka, & Muguruma, 1983), which has an optimumeffect on pH values near neutrality.

There were significant differences between the four age groupsof camels in myofibrillar fragmentation index in the present study(Tables 1 and 2). Cooled camel meat while still at pre-rigor condi-tion, cold shortening might take place. Therefore, the non-stimu-lated muscles might have undergone cold-shortening, which hasbeen shown to be associated with high shear force and low sarco-mere length. However, muscles from young camels were not af-fected by cold-shortening as much as for other age groups. Lowermyofibrillar fragmentation index and shorter sarcomere lengthfor the 10–12 years camels are consistent with the tougher meatfrom that group. The high myofibrillar fragmentation index in 1–3 year camels caused by easily breaking myofibrils into shortersegments may due to higher pH or proteolytic activity, which in-creases proteolytic activity and leads to rupture of the myofibrilsduring the 24 h post mortem storage.

3.6. Colour

Low voltage electrical stimulation tended to increase the CIE L*,a* and b* values which significantly (P < 0.05) improved the light-ness (L*) of muscles. King et al. (2004) and Riley et al. (1981) re-ported that meat from electrically-stimulated carcasses, have abrighter red colour than meat from non-stimulated carcasses.

Fig. 3. Micrograph from sections of electrically-stimulated and non-stimulated sections of camel Longissimus thoracis (magnification 30,000X): (A) electrically-stimulatedcross sections: muscle fibre bundles distorted and disintegrated (arrows), (B) non-stimulated cross section: dense packing of fibre bundles, (C) electrically-stimulatedlongitudinal section: spaces between fibres and disintegration at inter fibrillar bridges and (D) non-stimulated longitudinal section: pronounced transverse element (sampleswere taken immediately after electrical stimulation).

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Many factors including myoglobin concentration, ultimate pH, andmuscle fibre type, electrical stimulation and cooling rate influencethe development of muscle colour (Faustman & Cassens, 1990;MacDougall & Rhodes, 1972). Post mortem protein degradation isdirectly related to the ultimate pH, which increases light scatteringproperties of meat and thereby increases L*, a* and b* values (Offer,1991), which is also directly related to the pH (Abril et al., 2001).

Meat from 10–12 years camels was darker (lower L*), redder(higher a*) and yellowier (higher b*) than that of 1–3 years camels,while the other two age groups in between (Table 1). This darkercolour is more likely a result of increased myoglobin content (Law-rie, 1979), which increases with age. Other factors causing thisphenomenon include proportions of muscle fibre type and coolingrate (Abril et al., 2001; Faustman & Cassens, 1990). In the presentstudy, the older age group had a higher percentage of Type IIB fi-bres and lower percentage of Type I fibres than the younger agegroups (Table 3). The moderately high pH values from young cam-els (group 1) might have led to degradation of more protein. Abrilet al. (2001) reported that reflectance spectrum value for beef L.thoracis was higher with ultimate pH above 6.1. Mitochondrialactivity in post mortem muscles was increased by high tempera-tures and high pH values (Ashmore et al., 1972). This would in-crease oxygen consumption and therefore, decrease availabilityof oxygen in the meat, which in term increases the concentrationof deoxygenated myoglobin resulting in a dark colour (Lawrie,1979). The depth to which oxygen diffuses in meat depends onthe oxygen consumption rate by meat and the ambient tempera-ture (Ledward, 1992). More oxymyoglobin is formed at low tem-

peratures and at low pH values, conditions that increase oxygensolubility and inhibit oxygen consumption enzyme activity (Led-ward, 1992).

3.7. Muscle fibre types

Three different muscle fibres were observed in camel meat(Type 1 (bR), Type IIA (aR) and Type IIB (aW) (Fig. 2). The distribu-tion, diameters and relative area of three fibre types of L. thoracismuscle are shown in Table 3. Muscle fibre proportions wereaffected by age group (Table 3). The contractile type (fast or slow)as indicated by the slow/fast fibre ratio, decreased with increasingage. Type 1 significantly (P < 0.05) decreased and Type IIB in-creased with increasing age. According to Ashmore et al. (1972),transformation of Type I fibre types to Type IIB types, occurs duringpost-natal development in animals. There are many reports on therelationship between muscle fibre types and meat quantity andquality attributes. Ashmore (1974) suggested that transformationfrom Type I fibre types to Type IIB types might prove advantageousfor improving the quantity of meat, but be detrimental to quality.In the study of the L. thoracis muscle of lambs, chronological agewas positively correlated to Type I fibres and negatively correlatedwith Type IIB fibres (P < 0.05).

The fibre types Type I, Type IIA and Type IIB in 1–3 year-old ca-mel L. thoracis muscle were 29.94%, 40.13% and 29.93%, respec-tively (Table 3). Kassem, El-Sayed & Ahmed (2004) found thatthe mean percentages of Type I, Type IIA and Type IIB fibre typesin L. thoracis of 2 year-old camel muscle were 14.5%, 46.7% and

84 I.T. Kadim et al. / Meat Science 82 (2009) 77–85

38.8%, respectively. The differences between the current study andKassem, El-Sayed, and Ahmed (2004) study might be attributed todifferences in breeds, which suggest that Arabian camels have alarge variation in fibre types. Muscle fibre diameter and relativearea of fibre types was significantly different between the 1–3year-old camels and the other three age groups studied (Table 3).Similarly, Spindler, Matthias, and Cramer (1980) showed that fibrediameter increased with age or maturity. A little variability in mus-cle fibre diameter in each fibre was observed, however the relativearea was affected greatly by muscle fibre composition.

4. Conclusion

Electrical stimulation had a significant effect on meat qualitycharacteristics including pH, expressed juice, shear force value, sar-comere length, myofibrillar fragmentation index and colour of ca-mel L. thoracis muscles. These effects are due to ultrastructuralalteration and increased protein degradation. The age of the cameland ageing of meat had a significant influence on meat qualitycharacteristics and should be taken into consideration whenslaughtering camels for meat consumption.

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