Characterisation of the lipid and protein fraction of fresh camel meat and the associated changes during refrigerated storage

Accepted Manuscript Title: Characterization of the lipid and protein fraction of fresh camel meat and the associated changes during refrigerated storage Author: Sajid Maqsood Kusaimah Manheem Aisha Abushelaibi Isam Tawfik Kadim PII: DOI: Reference:

S0889-1575(15)00058-7 http://dx.doi.org/doi:10.1016/j.jfca.2014.12.027 YJFCA 2530

To appear in: Received date: Revised date: Accepted date:

4-8-2014 1-12-2014 17-12-2014

Please cite this article as: Maqsood, S., Manheem, K., Abushelaibi, A., and Kadim, I. T.,Characterization of the lipid and protein fraction of fresh camel meat and the associated changes during refrigerated storage, Journal of Food Composition and Analysis (2015), http://dx.doi.org/10.1016/j.jfca.2014.12.027 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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 High PUFA along with high amount of haem protein were found in camel meat

 TCA-soluble peptides, protein extractability and solubility increased during

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investigated

storage

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Highlights  Characterisation and changes of protein and lipid in camel meat were

 Continuous drip loss and drastic changes in texture and color were observed

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Original research article

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Characterization of the lipid and protein fraction of fresh camel meat and the associated changes during refrigerated storage

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Sajid Maqsood1*, Kusaimah Manheem1, Aisha Abushelaibi1, Isam Tawfik Kadim2

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Emirates University, Al Ain, 15551, UAE

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Sciences, Sultan Qaboos University, Sultanate of Oman

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To whom correspondence should be addressed: Tel: +97137134519; Fax:

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+97137675336

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Email: [email protected] (S. Maqsood)

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Abstract

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Department of Food Science, College of Food and Agriculture, United Arab

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Department of Animal and Veterinary Sciences, College of Agricultural and Marine

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fatty acids were reduced at the end of storage. Lipids underwent rapid oxidation as

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indicated by increase in peroxide value (PV) and thiobarbituric acid reactive

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substances (TBARS). Decrease in total haem pigment, myoglobin and haemoglobin

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content with concomitant decrease in redness (a* value) was noticed during the

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storage. Protein extractability, solubility, TCA-soluble peptides and drip loss

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Characterisation of protein and lipid fractions of fresh camel meat and their associated changes were investigated during 9 days of refrigerated storage. Camel meat lipids contained palmitic acid (C16:0) as dominant fatty acid followed by stearic acid (C18:0) and oleic acid (C18:1 n-9). Content of total saturated fatty acid (SFA) and unsaturated fatty acids were 58.46 and 41.5 mg/100g, respectively. Total unsaturated

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increased during storage indicating proteolysis and degradation of structural proteins,

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which was also evident from SDS-PAGE pattern. This further corroborates with the

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decrease of textural parameters like hardness, cohesiveness, springiness and

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gumminess. Thus, the protein and lipid fraction of camel meat underwent

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considerable changes during refrigerated storage. Therefore, the behaviour of protein

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and lipid fraction in camel meat during refrigerated storage could provide better

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understanding of the processing and storage conditions.

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Keywords: Camel meat; Food composition; Proteolysis; Fatty acid analysis; Protein

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characterisation; Lipid oxidation; Food analysis; Food processing

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1 Introduction

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With increasing demand for the meat and meat products due to increasing human

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population, there is an urgent need to look for marginal and underutilized options for

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the supply of red meat, such as those in semi-arid and arid lands, of which camel meat

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production is certainly the most suitable one. There are approximately 25 million

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camels in the world where the global market for camel products has a potential of US$10 billion a year based of Food and Agriculture Organization (FAO) of United Nations. United Arab Emirates is known to possess 412000 camels FAOSTAT, 2008). Camels are used for many purposes such as meat and milk production, and for physical labour as well as racing. Camel meat is known to be more beneficial for

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health because the meat contains lower fat and cholesterol levels than other red meats

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(Gheisari & Ranjbar, 2013). Camel meat is also relatively high in polyunsaturated

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fatty acid (PUFA) in comparison to other red meat (Gheisari & Ranjbar, 2013), which

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contributes to its health-promoting benefits. Consumption of camel meat can therefore

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lead to a reduction in total fat and cholesterol intake and an increase in PUFA as 3 Page 3 of 37

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compared with other conventional meat sources. Moreover, camel meat is also used

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for medicinal purposes in diseases such as hyperacidity, hypertension, pneumonia,

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and respiratory disease; it is also known as an aphrodisiac (Kurtu, 2004). Such a diet

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can be expected to reduce cardiovascular diseases and improve health (Rawdah, El

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Faer, & Koreish, 1994). Thus, camel as a meat source seems to present a viable

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alternative to other red meats.

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The compositional quality of fresh camel meat can be affected by problems

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encountered during refrigerated storage, i.e. lipid oxidation, discoloration, proteolysis

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and increase of drip loss, etc. Camel meat is the least studied meat and is mistakenly

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believed to be of lower nutritive value and quality than other types of red meat

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(Abdelhadi et al., 2013). Although camel meat is not universally consumed, it might

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be a potential alternative for meat, particularly in arid/semi-arid regions where camels

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can thrive well and are produced in a much more economical manner than cattle.

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Low-temperature storage is one of the primary preservation methods to maintain meat

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freshness, because the rates of microbiological, chemical and biochemical changes are

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refrigerated storage for varying periods to improve tenderness, the most important

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meat quality. Furthermore, during the retail display, the colour of the meat is affected

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significantly. All these quality attributes are related with the post-mortem changes in

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the protein and lipid fractions of the meat. Overall, there is a lack of research on

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camel meat to attain the better understanding of camel meat properties and their

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reduced at lower temperatures. Therefore, it is important to study and monitor the changes the meat undergoes during low-temperature storage. For instance postmortem refrigerated storage of meat, often termed as maturation or aging, permits desirable degradative structural changes in myofibrillar and connective tissue proteins which enhance its palatability (Takahashi, 1996). Meat carcasses are held in

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changes during refrigerated display. Some scientifically sound studies have been

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conducted concerning the physical characteristics, chemical composition and nutritive

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values of camel meat (El-Faer, Rawdah, Attar, & Dawson 1991; Elgasim and

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Alkanhal, 1992; Dawood and Alkanhal, 1995; Dawood, 1995; Kadim, Mahgoub, Al-

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Marzooqi, Al-Zadgali, Annamali, K., & Mansour, 2006; Kadim et al., 2013).

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However, there is no information available about the changes in protein and lipid

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fraction during refrigerated storage, which is very important to gain a better

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understanding of camel meat.

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Therefore, the aim of this research was to characterise the protein and lipid fractions

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and to study their associated changes in fresh camel meat during refrigerated storage.

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2 Materials and methods

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Chemicals

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Chloroform, ethanol, acetone and anhydrous sodium sulfate were obtained from BDH

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Prolabo (Briare, France). Methanol, sodium chloride, hydrochloric acid and glacial

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acetic acid were obtained from Scharlau Chemicals (Barcelona, Spain). Ammonium thiocyanate and trichloroacetic acid were procured from Panreac AppliChem (Barcelona, Spain). Iron (II) chloride and Coomassie brilliant blue R-250 was procured from AppliChem (Darmstadt, Germany). Cumene hydroperoxide (80% purity), thiobarbituric acid (>98% purity), 1,1,3,3-tetramethoxypropane (MAD) (99%

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purity), tyrosine (>98% purity), sodium phosphate dibasic, sodium dodecyl sulfate

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(SDS) (>98.5% purity), β-mercaptoethanol (β-ME), wide range molecular weight

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marker and bovine serum albumin (BSA) (>98% purity), were procured from Sigma-

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Aldrich Chemical Co. (St. Louis, MO, USA). All other chemicals used were of

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2.2

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Preparation of camel meat samples

Six female camels (Arabian dromedary one-humped camel, Camelus dromedarius),

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which had been reared in a semi-intensive management system and fed ad libitum on

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a Rhodes grass (Chloris gayana) hay diet mixed with date seed powder, were

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slaughtered at 3-5 years of age and when they had reached 410±25 k, at an Al Ain

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slaughterhouse in the United Arab Emirates (UAE). UAE-Standard No. 993/2000

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concerning animal slaughtering requirements according to Islamic law was followed

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to slaughter the camels. Semitendinosus (ST) muscle was carefully separated with a

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sharp knife from the carcass of the camels within 24 h of slaughter. Separated meat

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portions were packed in polyethylene bags and stored in insulated box filled with ice

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during transportation to laboratory of Department of Food Science, UAE University.

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Upon arrival, the meat was washed with chilled deionised water, cut into similar-sized

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pieces (3x3x3 cm), and the connective tissue and fat deposits were removed manually.

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Meat samples obtained from the carcass of the six female camels were divided into

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three batches (or replicates) and placed on separate polystyrene trays wrapped with

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shrink film. One portion from each batch or replicate was subjected to

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characterisation of protein and lipids, and another portion was used for studying the changes in protein and lipid fraction and assessing quality parameters during storage at 4 °C. During storage, the samples were taken and evaluated after every 3rd day up to 9 days.

2.3

Characterisation of lipid fraction of camel meat and its changes

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2.3.1 Lipid extraction and analysis of fatty acids composition

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Lipids from the fresh camel meat (day 0) and those stored for 9 days were extracted

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by the method of Bligh and Dyer (1959) using chloroform:methanol:distilled water

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mixture (50:100:50) as an extraction solvent. After extraction, the solvent was 6 Page 6 of 37

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evaporated at 25 °C, using an EYELA rotary evaporator N-100 (Tokyo, Japan), and

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the residual solvent was removed by flushing with nitrogen. Fatty acid profile of extracted camel meat lipids was determined as fatty acid

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methyl esters (FAMEs) as described by Maqsood and Benjakul (2010c). Supelco 37-

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Component FAME Mix (Sigma Aldrich, PA, USA, Cat No. 47885-U) was used for

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identification of different fatty acids. Fatty acid concentration was calculated by using

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C23 internal standards (purity >99%) (Sigma Aldrich, PA, USA). Average from the

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three runs was expressed as g fatty acid/100g lipid.

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2.3.2 Peroxide value (PV)

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Peroxide value (PV) of the camel meat was determined as per the method of Richards

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and Hultin (2002) with a slight modification. A standard curve was prepared using

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cumene hydroperoxide at the concentration range of 0.5-2 mg/kg. Peroxide value was

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expressed as mg of hydroperoxide/kg of sample.

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2.3.3 Thiobarbituric acid reactive substances (TBARS)

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TBARS in the camel meat were determined as described by Buege and Aust (1978).

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2.4.1 Determination of total haem pigment

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Total haem pigment in the camel meat was determined according to the method of

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Hornsey (1956) with some modification. A ground sample (10 g) was weighed into a

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50-mL polypropylene centrifuge tube. To this was added about half of an acidified

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acetone solution containing 40 mL of acetone, 9 mL of water (taking into account the

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A standard curve was prepared using 1,1,3,3-tetramethoxypropane (MDA) at the concentration ranging from 0 to 10 mg/kg and TBARS was expressed as mg of MDA equivalents/kg sample.

2.4

Changes in haem pigment

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amount of moisture in the meat) and 1 mL of HCl. Each sample was homogenised at

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13,500 rpm for 15 s using a Ultra-Turrax T25 high speed homogeniser (Janke &

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Kunkel, Staufen, Germany), and remaining acidified acetone solution was added. The

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samples were mixed thoroughly, and the tubes were capped tightly and allowed to

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stand in the dark for 1 h. The homogenate was centrifuged at 2200 g for 10 min at 4

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°C using a RC-5B plus centrifuge (Beckman, Je-Avanti, Brea, CA, USA). The

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supernatant was filtered with Whatman No.1 filter paper (Whatman International, Ltd,

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Maidstone, UK) and the absorbance was measured at 640 nm against a reagent blank

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using a UV-1601 spectrophotometer (Shimadzu Corporation, Kyoto, Japan). The

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absorbance was multiplied by the factor 6800 and then divided by the sample weight

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to give the concentration of total pigments in the meat as µg haematin/g meat (Turhan

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et al., 2004).

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2.4.2 Determination of haemoglobin content

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To determine haemoglobin content in the camel meat, haemolysate was prepared

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according to the method of Richard and Hultin (2002) with slight modification. In

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brief, 5 g of meat and 15 mL of 80 mM KCl were mixed with 50 mM Tris-HCl buffer (pH 8.0) in a polypropylene centrifuge tube. The sample was homogenised for 2 min at 3500 rpm, rinsed with additional 5 mL of the buffer and centrifuged at 3500g at 4°C for 30 min. The supernatant was referred to as haemolysate and used for quantification of haemoglobin. Haemoglobin content in the prepared haemolysate was

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determined following the method described by Maqsood and Banjakul (2011). The

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haemoglobin concentration was calculated by Lambert–Beer’s law using a millimolar

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extinction coefficient of 125 for oxyhaemoglobin at pH 8 (Antoni and Brunoni, 1971)

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and expressed in mM.

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2.4.3 Determination of myoglobin content

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Myoglobin content was determined by direct spectrophotometric measurement. A

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ground sample of (2 g) was weighed into a 50 mL polypropylene centrifuge tube and

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20 mL of cold 40 mM phosphate buffer, pH 6.8, were added. The mixture was

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homogenised at 13,500 rpm for 10 s, followed by centrifuging at 3000g for 30 min at

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4 °C, using a Allegra X 30R refrigerated centrifuge (Beckman Coulter, Brea,

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California, USA). The supernatant was filtered with Whatman No. 1 filter paper. The

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supernatant (2.5 mL) was treated with 0.2 mL of 1% (w/v) sodium dithionite to

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reduce the myoglobin and the absorbance was read at 555 nm. Myoglobin content was

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calculated from the millimolar extinction coefficient of 7.6 and a molecular weight of

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16,110 Daltons (Gomez-Basauri and Regenstein, 1992). The myoglobin content was

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expressed as mg/g sample.

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2.5

Characterisation of protein fraction

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2.5.1 Protein patterns by sodium dodecyl sulfate polyacrylamide gel electrophoresis (SDS-PAGE)

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Fresh camel meat (day 0) and those stored for 9 days were subjected to SDS–PAGE

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To determine protein extractability in camel meat, 10 grams of camel meat was mixed

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with 20 mL of 5% NaCl solution, homogenised for 5 min, incubated (4°C) for 1 h,

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and centrifuged at 30,000 × g (14,000 rpm) for 20 min (Gordon and Barbut, 1992).

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Biuret protein assay was used to determine protein concentration in the salt soluble

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protein extracts using bovine serum albumin (Sigma-Aldrich Chemical Co., St. Louis,

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according to the method of Laemmli (1970) as described by Maqsood and Benjakul (2010c). Wide range molecular weight markers ranging from 200 kDa to 20 kDa was used for estimation of molecular weight of proteins.

2.5.2 Determination of protein extractability, total protein solubility and TCA-soluble peptides

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MO, USA) as a standard. Protein extractability was expressed as mg of protein/g of

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sample. Total protein solubility was determined by the method described by Joo et al.

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(1999). Total proteins were extracted from 1 g camel meat using 20 mL of ice-cold

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1.1 M potassium iodide in 0.1 M phosphate buffer (pH 7.2). The samples were

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minced, homogenised on ice, and then left on a shaker at 4°C overnight. Samples

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were then centrifuged at 1500 g for 20 min, and protein concentration in the

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supernatants was determined by the Biuret method. Total protein solubility was

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expressed as mg of protein/g of sample.

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TCA-soluble peptides in the camel meat were determined according to the method

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of Morrissey et al. (1993). Meat samples (3 g) were homogenised with 27 mL of 5%

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TCA (w/v) at speed of 19,000 rpm using a homogeniser. Homogenate was kept in ice

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for 1 h and centrifuged at 5000g for 5 min. The soluble peptides in supernatant were

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measured by the Lowry method and expressed as mg of protein/g of sample.

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Changes in meat quality during refrigerated storage

2.6.1 Changes in pH of camel meat

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calibrated after every three readings using two buffers of pH 4.0 and 7.0.

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2.6.2 Colour determination

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Colour of the ground camel meat was measured using a Hunter Lab colorimeter

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(Model colour Flex, Reston, VA, USA) with the port size of 0.50 inch. The

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To determine pH, 10 g of the sample was homogenised with 50 mL of chilled distilled water. The pH values were measured with a portable digital pH meter attached with a probe (Model pH 510, Eutech Instrument, Ayer Rajah Crescent, Singapore). Three readings were taken by dipping the pH meter probe in the homogenate and mixing the homogenate on a magnet stirrer until the reading was stable. The pH meter was

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determination of colour was done on six different samples. Standardisation of the

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instrument was done using a black and white Minolta calibration plate. The colour

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values were calculated based on illuminant C and the 10° standard observer (CIE).

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The values were reported in the CIE colour profile system as L
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a
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value (yellowness/blueness) on day 0, 3, 6 and 9

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of storage.

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2.6.3 Drip loss

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The drip loss of the camel meat was calculated from differences in the weight taken

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before and after storage at 4°C and the results were expressed as average proportion

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(Honikel, 1998). The percent change in weight over the subsequent 48 h was taken as

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the drip loss, as described by Honikel (1998).

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Drip loss (%) = [(weightsample before cooling–weightsample after cooling)/(weightsample before

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cooling)]

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2.6.4 Textural profile analysis (TPA)

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TPA the camel meat cubes (3x3x3 cm) was performed using a texture analyser (CT3-

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4500, Brookfield Engineering Laboratories, Middleboro, MA, USA) with cylindrical aluminium probe (50 mm diameter) as described by Maqsood, Benjakul and Balange (2012). Hardness, springiness, cohesiveness, gumminess and chewiness were calculated from the force–time curves generated for each sample on day 0 and day 9 (Bourne, 1978).

2.7

Statistical analysis

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Meat portion removed from the carcasses of six different female camels were

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characterised and analysed for different parameters in triplicate. The experimental

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data were subjected to Analysis of Variance (ANOVA) and the significant differences 11 Page 11 of 37

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between mean values obtained at different sampling days were evaluated by Duncan’s

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Multiple Range Test/least significant difference (Steel & Torrie, 1980). Data analysis

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was performed using an SPSS package (SPSS 14.0 for Windows, SPSS Inc, Chicago,

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IL, USA).

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3 Result and discussion

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Characterisation and changes in lipid fraction of camel meat

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3.1.1 Changes in fatty acid profile of the camel meat lipids

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Semitendinosus (ST) muscle of the camels contains 4.82±0.84 % of total fat and

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71.77±3.84 % of moisture. Fatty acid profile of lipids extracted from fresh camel meat

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and those stored for 9 days at 4 °C is displayed in Table 1. Camel meat lipids (day 0)

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contained palmitic acid (C16:0) as dominant fatty acid followed by stearic acid

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(C18:0) and oleic acid (C18:1 n-9). Kadim et al. (2013) also reported that palmitic

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acid (C16:0) is the most abundant saturated fatty acid in camel intramuscular fat

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followed by stearic acid (18:0), and myristic acid (C14:0). The monounsaturated fatty

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acids (MUFA) contributed to about 30% of total fatty acids and among them oleic

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acid (C18:1n9c) followed by palmitoleic acid (C16:1) were the major ones. Rawdah et al. (1994) also reported that MUFA in camel meat account for almost one-third of the total fatty acids and are dominated by oleic acid followed by palmitoleic acid. Content of total saturated fatty acid (SFA) and unsaturated fatty acids were 58.46 and 41.5 mg/100g, respectively, indicating that camel meat lipids were dominated by

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saturated fatty acid with considerably high amounts of unsaturated fatty acids. Among

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the unsaturated fatty acid, camel meat lipid contain 29.23 mg/100g of mono-

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unsaturated fatty acids (MUFA) and 12.23 mg/100g of poly-unsaturated fatty acids

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(PUFA). High amount of unsaturated fatty acids (41.54 mg/100g) could play a major

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role in making the lipids more susceptible to lipid oxidation. The dominant PUFA in 12 Page 12 of 37

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the camel meat lipid was linoleic acid (Cis) (C18:2n6c). Kadim et al. (2013) also

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reported that the main polyunsaturated fatty acids in the muscles were linoleic acid

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(C18:2n6c). This finding further corroborates with those reported by Rawdah et al.

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(1994). These unsaturated fatty acids in camel meat lipids underwent oxidation during

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the refrigerated storage for 9 days. This was evidenced by the decrease in total

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unsaturated fatty acids from 41.54 to 39.89 mg/100g and PUFA from 12.23 to 9.75

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mg/100g on day 9 of storage. This was in agreement with the high formation of PV

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and TBARS in the camel meat on day 9 of storage (Fig. 1). Decrease in PUFA was

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coincidental with an increase in saturated fatty acids at the end of refrigerated storage.

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When comparing fatty acids between camel meat lipids at day 0 and day 9, there was

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a noticeable decrease in some of the PUFA especially C18:2n6, C18:3n6, C18:3n3

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and C20:4n6. PUFA reduction was due to oxidative and hydrolytic reactions that

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occurred during the storage. Yi-Chen et al. (2008) showed that long hydrocarbon

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chains and high unsaturation of PUFA made them more susceptible to hydrolytic

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reactions than the SFA. Decrease in PUFA resulted in corresponding increase of SFA

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when compared to the total fatty acid. Fatty acid composition of meat can play an

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al., (1996) reported that n-6/n-3 ratio of beef, lamb and pork meat was 2.11., 1.32 and

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7.22, respectively. The low n-6/n-3 levels are desirable for meat consumers’ health

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reasons (British Department of Health, 1994). Ratio of n-6/n-3 in camel meat lipids

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are very well in the recommended range of less than 4. Consumption of food with

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high proportion of MUFA and PUFA is related with lowering of serum cholesterol 13

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important role in determining the health benefits of meat to consumers. The ratio between n-6 and n-3 fatty acids have important role to play in reducing the risk of coronary heart disease (American Heart Association, 2008). Ratio of n-6/n-3 in the camel meat found in the present study is 3.96, which is within the range of recommended value of lower than 4 (British Department of Health, 1994). Enser et

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levels (Rawdah et al., 1994). Camel meat is known to contain higher percentage of

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MUFA and PUFA and lower cholesterol than beef, therefore, can be considered as an

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alternative healthy red meat.

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3.1.2 Changes in lipid oxidation products

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Changes in peroxide value (PV) and thiobarbituric acid reactive substances (TBARS)

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values of camel meat during refrigerated storage are shown in Figure 1 (a) and (b),

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respectively. A continuous increase in PV was observed in the sample during the first

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6 days. Thereafter, a sudden decreased in PV was noticed up to day 9 of storage

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(P<0.05). The results suggested that the camel meat underwent lipid oxidation at a

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pronounced rate during the first 3 days of storage. After 6 days of storage, the

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hydroperoxide formed might undergo decomposition to form secondary lipid

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oxidation products (Maqsood & Benjakul, 2010a). Therefore, a decrease in the

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peroxide value on day 9 was related to hydroperoxide degradation. Lee et al. (2010)

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reported that the peroxide value of the raw ground pork meat increased until 7 days

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and reached the maximum value at a certain storage time and decreased thereafter

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have overestimated the values. TBARS values of the camel meat increased as the

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storage time increased (P< 0.05) (Fig. 1b). The initial value of TBARS was 0.25

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mg/kg meat, suggesting that lipid oxidation had occurred during post-mortem

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handling to some extent. TBARS showed a marked increased within the first 3 days

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of storage indicating that camel meat was highly susceptible to lipid oxidation and

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during 14 days of refrigerated storage. Even though TBARS assay is widely used on the food laboratories for monitoring lipid oxidation in the food matrix, however, components like ketones, ketosteroids, acids, esters, sugar, protein and vitamins can react with TBA and thus can interfere with the assay (Devasagayam et al., 2003). In the present study, TBAR assay might

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lipids underwent oxidation rapidly during storage. TBARS showed a slight increase

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from days 3 to days 6 of storage (P>0.05). Thereafter, it increased sharply until the

330

end of storage (P<0.05). The increase in TBARS indicated formation of secondary

331

lipid oxidation products which contribute to the off-odour development in the meat.

332

The increases in TBARS were coincidental with the decrease in PV from 6 to 9 days

333

of storage. This was probably due to the degradation of hydroperoxides into

334

secondary oxidation products, especially aldehydes, in the later stages of lipid

335

oxidation (Maqsood & Benjakul, 2010b). Fallah, Tajik, & Farshid, (2010) also

336

reported that TBARS value of non-irradiated camel meat increases when storage time

337

increases for 15 day of refrigerated storage. Gheisari (2011) reported that the camel

338

meat showed the higher TBARS than cattle and chicken and the values increased with

339

an increase in storage time. Camel meat is known to contain high amount of

340

myoglobin and other haem compounds which function as pro-oxidants to promote

341

lipid oxidation (Maqsood & Benjakul, 2011). Therefore, the presence of high amount

342

of PUFA and pro-oxidants like haem pigment (myoglobin and haemoglobin) makes

343

camel meat highly prone to lipid oxidation.

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3.2

Changes in haem pigments in camel meat during storage

3.2.1 Changes in total haem pigment Changes in total haem pigment of camel meat during 9 days of refrigerated storage are shown in Figure 1(c). Total haem pigment is a measure of haematin, which is

348

related to haem containing proteins such as myoglobin, haemoglobin and cytochrome.

349

Total haem content of the fresh camel meat in this study was found to be 92.3 µg

350

haematin/g of sample which is higher than what was found in beef (76.16 3 µg

351

haematin/g of sample) (Maqsood & Benjakul, 2010b). Presence of high haem content

352

in the fresh camel meat might contribute to its susceptibility to lipid oxidation. Total 15 Page 15 of 37

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haem pigment gradually decreased as the storage time increased from day 0 to day 9

354

(P< 0.05). At day 0, total pigment of camel meat was 92.38 µg haematin /g meat and

355

it decreased to 86.4 µg haematin /g meat on day 9 of refrigerated storage. The

356

decrease could be due to the denaturation and oxidation of haem pigment during

357

storage. It was postulated that the haem pigment can display lower extraction

358

efficiency with increasing storage time which might have resulted in the decrease of

359

haem content of the meat (Chaijan, Benjakul, Visessanguan, & Cameron, 2005).

360

Decrease in total haem pigment during storage has been reported in different red

361

meats like lamb, beef and pork (Luciano, Monahan, Vasta, Pennisi, Bella, & Priolo,

362

2009; Maqsood & Benjakul, 2010b; Estevez, Ventanas, & Cava, 2007). Total haem

363

plays an important role in the colour fresh meat. Pigments in red meats like camel

364

meat are especially vulnerable to oxidation, which causes deep yellow or brown

365

discoloration during handling, chilling, and frozen storage. The decrease in haem

366

pigment during storage in the camel meat corroborates well with the decrease in

367

redness (a*) values (Table 2). The decrease of haem pigment during storage can also

368

play an important role in the lipid oxidation of the meat. Damage and denaturation of

370 371 372

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the haem pigment with increasing storage time results in the release of iron which can accelerate lipid oxidation (Maqsood & Benjakul, 2010b). 3.2.2 Changes in myoglobin and haemoglobin Myoglobin and haemoglobin content of camel meat during 9 days of refrigerated

373

storage are shown in Figure 1 (d). Haemoglobin and myoglobin are known to be

374

potent catalysts of lipid oxidation in muscle foods (Maqsood and Benjakul, 2011). In

375

the present study, average myoglobin content of the camel meat was 7.16 mg/g of

376

sample. Ghesari (2011) reported that camel meat contain myoglobin content of 3.64

377

mg/g of sample. The lower myoglobin content in the study of Ghesari (2011) might 16 Page 16 of 37

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be due to the different extraction solvent and extraction conditions used. Moreover,

379

the portion of the camel carcass used in the study of Ghesari (2011) was different than

380

ours. In the present study, an increase in myoglobin and haemoglobin content were

381

observed in the camel meat on the day 3 of storage. Thereafter, a continuous decrease

382

in myoglobin and haemoglobin content was noticed up to day 9 of storage (P<0.05). It

383

was reported that the lower tendency of the haem proteins (haemoglobin and

384

myoglobin) towards extraction when the storage time is increased might have

385

resulted in their lower content in the meat (Chaijan et al., 2005). With the increase of

386

storage time, high degree of haem destruction might have taken place, which could

387

resulted in lower extraction of haemoglobin and myoglobin from the camel meat,

388

which could have ultimately resulted in release of more iron from the prophyrin ring

389

of haemoglobin and myoglobin, thus acting as pro-oxidants in the camel meat during

390

the storage. Until now no study has reported the haemoglobin content in the camel

391

meat. Knowledge regarding amount of haemoglobin present in the camel meat is

392

important, as it plays an important role as a pro-oxidant in the meat. After the animal

393

is being slaughtered, the iron atom in the haem ring of the haemoglobin or myoglobin

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(Maqsood & Benjakul, 2011). Therefore, the presence of myoglobin and haemoglobin

400

in the camel meat can be a decisive factor in making the lipids more prone to lipid

401

oxidation.

394 395 396 397

is primarily in the ferrous (+2) state. Conversion of ferrous haemoglobin or myoglobin to met (+3) haemoglobin or myoglobin is a process known as autoxidation. Autoxidation appears to be a critical step to enhance lipid oxidation since met haemoglobin or met myoglobin reacts with peroxides to stimulate the formation of compounds capable of initiating and propagating lipid oxidation

17 Page 17 of 37

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3.3

Maqsoodet al.

Characterisation and changes in protein fraction of camel meat

3.3.1 Changes in protein pattern by SDS PAGE

404

Changes in protein pattern of camel meat during 9 days of refrigerated storage are

405

presented in Figure 2. Camel meat protein contains myosin heavy chain (200

406

Kilodaltons; KDa), C-protein (140 KDa), Alpha actinin (110 KDa), tropomysin (70

407

KDa), and actin (55KDa). C-protein is a thick filament of a single polypeptide chain

408

having a molecular mass of 140 KDa. α-Actinin is located exclusively in the Z disk

409

and has a molecular mass of 130 KDa. Tropomyosin is a protein with two-stranded

410

coiled-coil of an α-helix having a molecular mass of 65-70 KDa. Actin is a major

411

protein of the thin filaments in the meat, which comprises 15-30% of myofibrillar

412

protein of muscle and had a molecular mass of 43-48 KDa (Abdelhadi et al. 2013).

413

During the storage at refrigerated temperature for 9 days, different proteins in the

414

camel meat underwent degradation to some extent as depicted in Figure 2. MHC, C-

415

protein, alpha actinin as well as tropomyosin bands showed a noticeable degradation

416

on day 9 of storage. Proteolytic degradation of myofibrillar proteins, especially

417

myosin, might result in the loss of structural domains of the meat (Takahashi, 1996),

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proteins as well as due to the production of endoproteinases by microorganisms.

424

Oxidation of proteins is believed to cause protein fragmentation and degradation of

425

structural protein (Maqsood and Benjakul, 2010b). Proteolysis by endogenous

426

proteases in the meat during storage might be associated with the pronounced

427

microbial growth (Maqsood & Benjakul, 2010b; 2010c). It is well established that the

418 419 420 421

which is reflected by the lower hardness values obtained in the camel meat on day 9 of storage (Table 2). Ageing or storage of meat at refrigerated temperature is the period during which an increase in tenderness and specific degradation of structural proteins occurs (Kadim et al., 2006). Degradation of different protein bands in the camel meat during the refrigerated storage might also be due to the oxidation of

18 Page 18 of 37

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proteolysis of myofibrillar proteins by endogenous proteases during post-mortem

429

aging is primarily responsible for the tenderisation of meat. The principal degradative

430

change in proteins that occurred over 9 days of storage, as detected by SDS-PAGE,

431

was the appearance of troponin T (30KDa) band. Loss of troponin T has been related

432

to protein degradation and could play a role in tenderness (Gheisari, Aminlari, &

433

Shekarforoush, 2009). Therefore, the camel meat proteins underwent degradation to

434

some extent during the refrigerated storage of 9 days.

435 436

3.3.2 Changes in protein extractability, protein solubility and TCAsoluble peptides

437

Extractability of camel meat protein during refrigerated storage is shown in Figure 3.

438

Extraction of proteins was carried out in 5% NaCl as an extraction solvent. Extraction

439

of myofibrillar proteins, commonly called salt-soluble proteins, is crucial in

440

manufacturing of further processed meat products such as frankfurters and bologna.

441

Once extracted, these proteins serve as emulsifying agents in meat batter and

442

contribute to emulsion stability and play an important role during processing of

443

restructured meat products (Hultin, Feng, & Stanley, 1995).

445 446 447

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Extractability of camel meat proteins did not changed significantly during the first 6 day of storage (P>0.05). Thereafter, an increase in protein extractability was noticed up to day 9 of storage (P<0.05). During the early period of storage, myofibrillar protein could apparently form an insoluble fraction due to denaturation that accounts

448

for the lower protein solubility and thus extractability (Leelapongwattana, Benjakul,

449

Visessanguan, & Howell, 2005). Degradation of myofibrillar proteins, commonly

450

called salt-soluble proteins, during the extended storage period might have resulted in

451

high extraction of total protein. Extractability behaviour of proteins from camel meat

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has not been reported before. The amount of protein extracted will play an important

453

role in the performance of its functional properties.

454

Solubility of protein is one of the most important physicochemical property through

455

which protein performs its different functional properties like emulsifying, foaming,

456

gelling (Kristinsson & Rasco, 2000). In the present study, solubility of camel meat

457

protein on day 0 was 9.4 mg/g of sample and it increased to 12.6 mg/g on 9 days of

458

storage (P<0.05) (Figure 3a). The increase in protein solubility with the increasing in

459

storage time might have resulted in higher values for protein extractability. The

460

protein solubility changes were due to myofibrillar protein degradation. Protein

461

solubility is used as an indicator of protein denaturation, and low protein solubility

462

indicated a high extent of protein denaturation (Joo et al. 1999).

463

Changes in TCA-soluble peptides in camel meat sample during 9 days of refrigerated

464

storage are shown in Figure 3b. TCA-soluble peptides showed a sharp increase

465

throughout 9 days of refrigerated storage (P<0.05), suggesting the autolytic

466

degradation of meat protein resulting in the release of peptides. This indicates that

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472

& An, 1997).

467 468 469 470

endogenous enzymes were active enough during the refrigerated storage to cause the breakdown of proteins to peptides. The action of proteolytic enzymes such as calpains and cathepsins on the myofibrillar protein fraction results in the production of protein fragments like that of TCA-soluble peptides. TCA-soluble peptide has been used as the index for the protein degradation of muscle food (Benjakul, Seymour, Morrissey,

20 Page 20 of 37

JFCA-D-14-00457

3.4

Changes in quality parameters of camel meat during refrigerated storage

3.4.1 Changes in pH

476

Changes in pH of fresh camel meat during 9 days of refrigerated storage is shown in

477

Figure (4a). Initial pH value of fresh camel meat was 6.2. Soltanizadeh, Kadivar,

478

Keramat and Fazilati (2008) also reported that the pH of camel meat was 6.15 after 12

479

h post-mortem. The range of pH in the camel meat during the refrigerated storage was

480

from 6.2 to 5.4, which were within the range for camel meat (6.16 to 5.83) reported

481

by Eskandari, Majlesi, Gheisari, Farahnaky and Khaksar (2013). There was an abrupt

482

decrease in pH on day 3 of storage (p<0.05), after which the decrease was gradual

483

until the end of storage period (p>0.05). This is usually due to the fact that camels

484

possess high gluconeogenesis capacity because of the presence of camel hump, which

485

cause rapid drop of pH (Soltanizadeh et al., 2008). The decline of pH in meat depends

486

on the amount of glycogen in the muscle at the time of slaughter. Lower glycogen

487

contents result in decreased rates of anaerobic glycolysis; therefore, a slower

488

production of lactic acid and hence a lower rate of post-mortem pH decline

489 490 491 492 493

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Maqsoodet al.

(Soltanizadeh et al., 2008). Camel meat reached to an ultimate pH of 5.4 after 9 days of storage. The range of the ultimate pH values of dromedary camel meat ranged between 5.7 and 6.0 (Kadim et al., 2006). The rate and extent of post-mortem pH decline may induce protein denaturation, affecting tenderness, WHC, juiciness and colour, thus plays an important role in quality of camel meat.

494

3.4.2 Changes in textural properties of camel meat

495

Texture profile analysis of the camel meat at day 0 and 9 of refrigerated storage is

496

shown in Table 2. Hardness, springiness, gumminess and chewiness values of camel

497

meat samples sharply decreased from day 0 to 9 of refrigerated storage, while there

498

was no significant change in cohesiveness. There was an increase in cohesiveness of 21 Page 21 of 37

Maqsoodet al.

the camel when stored for 9 days under refrigeration (P<0.05). The major eating

500

qualities of meat are developed during muscle aging, and it is well established that

501

aging or storage improves meat tenderness and thus the eating quality. Normally,

502

increasing the aging time will also increase tenderness, and water-holding capacity is

503

closely related to meat tenderness during aging. In this study, decrease in hardness,

504

gumminess, chewiness, and springiness in the camel meat during the storage was

505

supported by the increased drip loss and decreased water-holding capacity. Softening

506

of camel meat occurred after storage of 9 days, which could probably be due to the

507

proteolytic action promoted by muscle endopeptidases (calpain I and II and cathepsin

508

B, D, H and L).

509

3.4.3 Changes in colour parameters

510

Changes in L* (lightness), a* (redness) and b* (yellowness) of camel meat kept under

511

refrigerated storage for 9 days are presented in Table 2. Results showed that L* value

512

increased as storage time increased, while a* and b* values showed a gradual

513

decrease throughout 9 days of storage (P<00.5). Redness (a*) value of camel meat

514 515 516 517 518

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JFCA-D-14-00457

decreased drastically during first 6 days of storage from an initial value of 19.98 to 11.58 (P<0.05). Red colour of the meat is due to the presence of myoglobin pigment. Decrease in redness (a*) values in the camel meat with an increase in storage period was in agreement with decrease in total haem pigment and myoglobin content during storage (Fig. 2). Decrease in redness occurs in all types of meat, which is mainly due

519

to oxidation of oxy-myoglobin to form metmyoglobin (Maqsood & Benjakul, 2010b).

520

During the post-mortem storage of meat, myoglobin in the ferrous state is oxidized to

521

ferric metmyoglobin, resulting in a brownish-red meat (Maqsood & Benjakul, 2010b).

522

Guidera et al. (1997) reported that redness (a*) values in lamb meat tended to

22 Page 22 of 37

Maqsoodet al.

decrease during chilled storage. High oxygen packing with added natural antioxidants

524

can be used as a strategy to retain the redness of camel meat during storage.

525

3.4.4 Drip loss

526

Drip loss of camel meat kept under refrigerated storage for 9 days is shown in Figure

527

4 (b). The ability of meat to retain inherent water, defined as water-holding capacity

528

(WHC), is an essential quality parameter for both the industry and the consumer. Drip

529

loss is considered to be inversely proportional to WHC. For the meat processing, the

530

WHC of fresh meat is known to influence its technological quality, i.e. processing

531

yield. In the present study, a continuous increase in drip loss was observed in the

532

camel meat when the storage time increased (P<0.05). This might be due to a greater

533

loss of water holding property of the muscle protein. The increase in drip loss with

534

storage time is explained by water loss from the muscle due to degradation of muscle

535

proteins caused by the spoilage mechanisms. WHC or drip loss is affected by

536

degradation of myofibrillar proteins (Traore et al., 2012). Abdelhadi et al., (2013) also

537

reported that the drip loss in the camel meat continuously increased during

538 539 540 541 542

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JFCA-D-14-00457

refrigerated storage for 7 days. As the camel meat aged, protein might have undergone denaturation, which might have resulted in its loss of water holding capacity. Severe denaturation affects the protein's ability to bind water and thus results in high drip loss (Traore et al., 2012). The high drip loss is considered to be a serious quality problem because it contributes to the lower acceptability due to the

543

fewer taste constituents remained as well as the shrinkage of the meat.

544

4 Conclusions

545

The present study showed that the camel meat contains high quantities of unsaturated

546

fatty acid with significant amount of health-promoting PUFA. However, the presence 23 Page 23 of 37

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of PUFA along with high haem proteins (Hb and Mb) could make camel meat more

548

prone to lipid oxidation as reflected by high PV and TBARS formation. There was a

549

considerable change in the protein fraction of camel meat during storage. Degradation

550

of protein bands with concomitant increase in TCA-soluble peptides and protein

551

extractability and solubility was evident after 9 days of storage. Camel meat showed a

552

gradual deterioration of composition quality attributes, which includes a continuous

553

drip loss and drastic changes in texture profile and colour. Nevertheless, developing

554

diverse products from camel meat through optimum processing, proper preservation

555

and consumer acceptance can be a future research focus in order to popularize camel

556

meat among the consumers.

557

Acknowledgements

Authors are thankful to United Arab Emirates University for the funding this research

559

through a research grant (No. 31F024).

560

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compounds on In vitro antioxidative activity and the preventive effect on lipid

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oxidation of fish oil emulsion and fish mince. Food Chemistry, 119, 123-132. Maqsood, S. & Benjakul, S. (2010b). Preventive effect of tannic acid in combination

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with modified atmospheric packaging on the quality losses of the refrigerated

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ground beef. Food Control, 21, 1282-1290.

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661

Maqsood, S. & Benjakul, S. (2010c). Synergistic effect of tannic acid and modified

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atmospheric packaging on the prevention of lipid oxidation and quality losses

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of refrigerated striped catfish slices. Food Chemistry, 121, 29-38.

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Maqsood, S. & Benjakul, S. (2011). Comparative studies on molecular changes and

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pro-oxidative activity of haemoglobin from different fish species as influenced

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by pH. Food Chemistry, 124, 875-883.

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Maqsood, S., Benjakul, S., & Balange, A.K. (2011). Effect of tannic acid and kiam

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wood extract on lipid oxidation and textural properties of fish emulsion

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Morrissey, M. T., Wu J. W., Lin D., & An H. (1993) Protease inhibitor effects on torsion measurements and autolysis of Pacific whiting surimi. Journal of Food Science, 58, 1050–1054

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to lipid oxidation in fish muscle. Journal of Agricultural and Food Chemistry,

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beef and camel meat proteolysis during cold storage. Meat Science, 80, 892-

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Takahashi, K. (1996): Structural weakening of skeletal muscle tissue during postmortem ageing of meat: the non-enzymatic mechanism of meat

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tenderisation. Meat Science, 43, 67-80.

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700 701 702 703

Figure 1. Changes in peroxide value (a); thiobarbituric acid reactive substances (b); total haem pigment (c) and myoglobin and haemoglobin content (d) in camel meat during refrigerated storage. Values are mean±SD from 18 determinations. Different letter at different storage time indicates the significant difference (p<0.05).

704 705

Figure 2. Proteolysis in the camel meat proteins as determined by sodium dodecyl sulfate- polyacrylamide gel electrophoresis (SDS-PAGE).

706 707 708 709

Figure 3. Protein solubility (a) and protein extractability and TCA-soluble peptides (b) in camel meat proteins as affected by refrigerated storage. Values are mean±SD from 18 determinations. Different letter at different storage time indicates the significant difference (p<0.05).

710 711 712

Figure 4. Changes in pH (a) and drip loss (b) in the camel meat during refrigerated storage. Values are mean±SD from 18 determinations. Different letter at different storage time indicates the significant difference (p<0.05).

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713

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714

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TBARS (mg MDA/kg sample)

4

a

3

c

b

2

c

1 0

0

6

9

cr

b )

3

Storage time (Days)

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714

717 718 719 720

d )

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715 716

a )

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b

Figure 1

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Figure 2

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744 745 746 747

d

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cr

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721 723 725 727 729 731 733 735 737 739 741 743

33 Page 33 of 37

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a)

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b) Figure 3

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747 748 749 750 751 752 753 754 755 756 757 758 759 760 761 762 763 764 765 766 767

Maqsoodet al.

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34 Page 34 of 37

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a b

b

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c

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a)

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Figu re 4

d

b)

Ac ce p

767 768 769 770 771 772 773 774 775 776 777 778 779 780 781 782 783 784 785 786 787 788 789 790 791 792 793

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Table 1. Changes in fatty acid composition of lipids extracted from camel meat on

794

day 0 and day 9 of refrigerated storage.

822

9 Day

0.39±0.094 a 0.16±0.069 a 0.71±0.084 b 5.88±1.98 a 1.99±0.13 b 29.64±2.74 a 1.98±0.15 a 16.56±2.15 a 1.15±0.097

Tetradecenoic acid Ginkgolic acid Palmitoleic acid Ginkgolic acid Oleic acid

0.43±0.079 a 0.47±0.077 a 3.15±1.51 b 0.79±0.094 b 24.48±2.45

a

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d

802 0.44±0.083 a 0.56±0.82 a 3.07±1.49803 a 0.92±0.099 804 a 25.17±2.55 a

us a

2.23±0.25 a 3.46±0.26 a 2.03±0.198 a 1.90±0.12 a 0.08±0.006 b 0.21±0.007 a 1.87±0.118 a 0.14±0.008 a 0.31±0.009 58.46 41.54 29.32 12.23 3.96

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Linoleic acid (trans) Linoleic acid (Cis) Gamma Linolenic acid Alpha Linolenic acid Eicosadienoic acid Eicosatreinoic acid Arachidonic acid Docosadienoic acid Docosahexaenoic acid

a

796 a

0.36±0.090 a 797 0.17±0.071 a 0.68±0.088 798 a 6.19±1.99 a 1.94±0.12799 a 30.33±2.95 a 1.97±0.14800 a 16.94±1.95 a 801 1.53±0.099

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Capric acid Lauric acid Tridecylic acid Myristic acid Pentadecylic acid Palmitic acid Margaric acid Stearic acid Arachidic acid

795

cr

0 Day

805 b 2.07±0.23806 b 3.01±0.25807 b 1.39±0.198 b 808 1.34±0.106 a 809 0.07±0.004 a 0.29±0.009 810 b 1.22±0.119 811 a 0.15±0.009 a 812 0.21±0.008 813 60.11 39.89 814 30.16 815 9.75 816 4.17 817

Values are mean±SD from 3 determinations. Different letters in the same row for each fatty acid at different storage time denote the significant difference (P<0.05).

Ac ce p

818 819 820 821

Common name

te

Fatty Acids Saturated FA C10:0 C12:0 C13:0 C14:0 C15:0 C16:0 C17:0 C18:0 C20:0 Mono-unsaturated FA C14:1 C15:1 C16:1 C17:1 C18:1 n-9 Poly-unsaturated FA C18:2n6t C18:2n6c C18:3n6 C18:3n3 C20:2 C20:3n3 C20:4n6 C22:2 C22:6n3 Total Saturated FA Total Unsaturated FA Total mono-unsaturated FA Poly-unsaturated FA Ratio of n-6/ n-3

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Table 2

823

Changes in textural properties and colour values of camel meat during 9 days of Hardness (g)

Cohesiveness

time (days)

Springiness

Gumminess (g)

(mm)

Chewiness (mJ)

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Storage

3228±39.60a

0.61±0.01b

6.4±0.1a

2235±17.07a

146.39±5.01a

9

927.5±23.03b

0.73±0.02a

5.30±0.22b

774.1±27.98b

40.13±4.98b

L*

a*

b*

0

34.44±0.42c

19.98±1.48a

17.78±1.05a

3

35.46±1.23c

16.73±0.66b

15.72±0.91b

6

37.59±1.14a

12.81±0.46c

15.03±0.66cb

9

38.83±0.11b

11.58±0.72d

14.75±0.04c

Colour values

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0

us

Textural properties

refrigerated storage.

825 826 827

For textural properties and for colour values are mean ± SD (n=18). Different letters in the same column for each parameter at different storage time denote the significant difference (P<0.05).

an

824

Ac ce p

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d

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828

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