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Small Ruminant Research 78 (2008) 1–12

Effect of rearing system on some meat quality traits and volatile compounds of suckling lamb meat Mar´ıa Teresa Osorio a , Jos´e Mar´ıa Zumalac´arregui a , Enrique Alfonso Cabeza b , Ana Figueira c , Javier Mateo a,∗ a

Department of Food Hygiene and Technology, University of Leon, Campus Vegazana s/n, 24071 Le´on, Spain b Department of Microbiology, Faculty of Sciences, Campus Universitario, Km 1, v´ıa Bucaramanga, Edificio Sim´on Bol´ıvar, Pamplona, N. de S/der, Colombia c School of Technology, University of the Algarve, Campus da Penha, 8005-139 Faro, Portugal Received 23 November 2007; received in revised form 8 March 2008; accepted 18 March 2008 Available online 19 May 2008

Abstract Twenty Churra-breed suckling lamb carcasses from two groups of animals were used in this study. One group had been reared on maternal milk (MM), and the other had been reared on milk replacer (MR) until slaughter at 25–35 days old. The effects of the type of milk on several meat quality traits were studied. These effects included pH, colour, WHC, texture, retinol and tocopherol concentrations, colour and lipid oxidation stability, and the volatile compounds that formed during boiling of the meat. Furthermore, a sensory analysis (triangle test) was carried out. The colour of M. longissimus dorsi of MM samples showed higher L*, lower a*, and higher b* values than those of MR samples (P < 0.05). Retinol, ␣-, ␦- and ␥-tocopherol levels were all higher in the meat of lambs reared on MM (P < 0.001). Rancimat tests and TBARS analysis revealed more lipid-oxidative stability for the meat of the MR group, and the colour of meat from this group was also more stable. Likewise, volatile compounds derived from lipid oxidation were more abundant in the MM samples than in the MR group samples. The presence of volatiles attributed to non-oxidative lipid thermal degradation also differed between the two rearing systems, with concentrations of volatiles derived from dodecanoic acid being clearly higher for the MR meat samples. Residues of butylated hidroxytoluene (BHT) were detected in MR samples but not in the samples of the MM treatment. In the triangle test, an untrained panel could not detect a significant difference between MM and MR meat samples. The present study has demonstrated that variation in the composition of milk sources (MM vs. EM) used in rearing suckling lambs may be responsible for a significant effect in oxidative stability of fresh suckling lamb meat during storage and display and in the volatile composition of cooked suckling lamb meat. Thus, meat from MR-fed suckling lambs may become more stable to oxidation compared to meat from MM-fed suckling lambs. MR-reared meat may, however, have a different flavour from what is expected from the more traditional MM-fed suckling lamb meat. © 2008 Elsevier B.V. All rights reserved. Keywords: Suckling lamb; Milk replacer; Meat quality; Volatile compounds; Lipid oxidation stability; Colour deterioration

1. Introduction

∗

Corresponding author. Tel.: +34 987291247; fax: +34 987291284. E-mail address: [email protected] (J. Mateo).

0921-4488/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.smallrumres.2008.03.015

In Mediterranean countries, consumers prefer meat from light lambs fed either milk or mainly concentrate diets (Vergara et al., 1999; Sa˜nudo et al., 2006). Among light lambs, suckling lambs are the lightest on the market

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and have tender and juicy meat that shows a pearly white to pale pink colour and that is smooth in texture with a distinctive flavour (Gorraiz et al., 2000). Suckling lambs are reared exclusively on either maternal milk (MM) or milk replacer (MR). Several recent studies have addressed the effect of milk source on suckling lamb meat quality (Napolitano et al., 2002; Vicenti et al., 2004; Lanza et al., 2006; Napolitano et al., 2006; Osorio et al., 2007a,b,c). In these studies, physico-chemical characteristics of lipid fraction, proximate and mineral composition of meat, pH, colour, texture, and water-holding capacity (WHC) have been investigated as quality traits. Among them, the major emphasis has been on the fatty acid profiles of suckling lamb tissues, which have appeared to be strongly affected by dietary fat composition. This effect has been observed not only when using different milk sources (MM or MR) for feeding suckling lambs but also when using exclusively MM but different ewe feeding systems (Valvo et al., 2005). In addition, differences were found in the mineral composition and colour between the meat from MM- or MR-reared lambs. In spite of the work reported above, how feeding suckling lambs with MM or MR will affect some other major lamb meat quality traits such as lipid oxidation, meat discolouration, and flavour generation during cooking is not well understood. The current study was conducted to determine the effect of milk type on several technological quality traits of suckling lamb meat. Some of these traits have been previously studied (e.g., pH, colour, texture, WHC), and others have not been studied before (e.g., vitamin content, volatile composition, lipid oxidation, and colour deterioration of meat during chilled storage). In addition, a sensory analysis (triangle test) was conducted. 2. Materials and methods 2.1. Animals and sampling A total of 20 suckling lambs reared at a farm affiliated with a Churra breeders association from Castilla y Le´on, Spain were used in the experiment. Of the 20 lambs, 10 were reared on MM, and the other 10 were reared on MR until slaughter (between 25 and 35 days old). Animals and carcasses were the same as those described in a previous study (Osorio et al., 2007c). Means (±standard deviations) for carcass weights of the MM and the MR groups were 5.36 ±0.57 and 5.89 ±0.93 kg, respectively. Carcasses were transported under refrigerated conditions to the laboratory, where they were split into two halves and the leg of each half carcass was separated (Colomer-Rocher et al., 1988). Pelvic fat and bones were removed from the legs (Fisher and De Boer, 1994), and the leg meat was frozen and stored at −40 ◦ C until further analysis (between 1 and 6 months).

Moreover, longissimus dorsi muscle and kidney knob channel fat (KKCF) were dissected from the leg-less carcasses. In addition, the MR and the MM used for feeding the animals on the farm were sampled twice and analysed for vitamin content. 2.2. Physico-chemical characteristics in M. longisssimus dorsi Analyses of expressible juice, pH, haem pigment content, and moisture and fat content in the M. longissimus dorsi portion between the 6th and 10th ribs were carried out less than 48 h after slaughter. Expressible juice was determined in triplicate, according to the methods of Grau and Hamm (1957) from small strips (approximately 300 mg) of fresh meat cut parallel to the muscle fibres. After that, the M. longissimus dorsi portions from both halves of the carcass were homogenized together and pH was measured using a pH meter (Model 507; Crison, Barcelona, Spain) equipped with a puncture electrode (Model 52-32; Crison). In addition, haem pigment content was determined according to the method described by Hornsey (1956), and moisture and intramuscular fat (IMF) percentages were assessed according to the ISO R-1442 (1973) and AOAC method number 991.36 (AOAC, 1999), respectively. Other analyses were carried out on M. longissimus dorsi portions between the 11th and 13th ribs (also less than 48 h after slaughter). The intact portions (right and left side) were used for colour determination using a CM-500 chromometer (Konica Minolta, Osaka, Japan). Colour measures were taken in the CIE L*a*b* colour space (illuminant: D65; visual angle: 10◦ ; SCI mode; 11 mm aperture for illumination and 8 mm for measurement; chromometer calibrated with the white calibration tile provided with the equipment), following the methodology described by Honikel (1997). Prior to colour determination, samples were allowed to bloom at room temperature for 60 min, and then colour was measured in duplicate with the chromometer touching down directly onto each of the samples’ cross-section surfaces. Next, right and left M. longissimus dorsi portions were separately wrapped in aluminium foil, placed in plastic bags, and frozen for 5 months at −40 ◦ C until further analysis. After thawing (48 h at 4 ◦ C), the right muscle portions were cooked in a water bath at 75 ◦ C until reaching a core temperature of 70 ◦ C, and they were then cooled for 30 min at room temperature to determine water loss (cooking loss; Honikel, 1997). Afterwards, the cooked sample portions were wrapped in an oxygen permeable polyvinyl-chloride (PVC) film (14,000 ml/(m2 24 h)) and held overnight at 4 ◦ C. Subsequently, two to three rectangular prisms (1 cm × 1 cm × 2.5 cm long), with the long side cut parallel to muscle fibre orientation were obtained manually (using 1-mm-square-size linear graph paper and a scalpel) from each sample. Shear force was evaluated using a texture analyzer (TA-XT2i, Texture Technologies Corporation, Scarsdale, NY, USA) equipped with a Warner–Bratzler device, which operated at a cross-head speed of 100 mm/min, using a 25-kg load cell, and with the sample

M.T. Osorio et al. / Small Ruminant Research 78 (2008) 1–12

prisms being sheared at right angle to the fibre axis (Honikel, 1997). For the analysis of vitamins A and E, IMF was first extracted from each of the M. longissimus dorsi left sections (Bligh and Dyer, 1959). Vitamins were then extracted from the IMF following methods described by Yang et al. (1992) with slight modifications. Duplicate IMF aliquots (0.25 g) were saponified using 1 ml of 20% methanolic KOH at 68 ◦ C for 45 min, and vitamins were extracted twice with 3 ml of diethyl ether. The extracts were combined and washed three times with 3 ml of water. Ether was removed under nitrogen at room temperature, and the residue was dissolved in 1 ml of methanol. Separation of vitamins by HPLC was carried out using a Separation Module (Waters 2690; Waters Corporation, Milford, MA, USA) equipped with a Photodiode Array (Waters 996) detector and a C18 column, 250 × 3.0 mm i.d. (OmniSphere 5; Varian Inc., Palo Alto, CA, USA). Chromatographic conditions were as described by Rodas-Mendoza et al. (2003). Elution was performed with 100% methanol as mobile phase at a flow-rate of 1 ml/min, with the column kept at 50 ◦ C during analysis. Detection of ␣-, ␥-, and ␦tocopherols was performed at 292 nm, and retinol was detected at 325 nm. Chromatographic peaks were identified by comparing retention times and spectra (210–500 nm) of samples with those of standards (Sigma–Aldrich Sigma–Aldrich Qu´ımica, Madrid, Spain; standard names and reference numbers: dl␣-tocopherol, 47783; ␦-tocopherol, 47784; (+)-␥-Tocopherol, 47785). Quantification was assessed using calibration curves obtained with known amounts of the standards after being subjected to the same processing as for the IMF samples, as mentioned above. 2.3. Physico-chemical characteristics in kidney knob channel fat and leg meat of suckling lambs Fat colour was determined on the surface of an intact portion of fresh KKCF (more than 2 cm wide) before 48 h post-mortem, in the CIE L*a*b* colour space using the same chromometer, parameters and conditions previously mentioned. Frozen leg meat samples were thawed (48 h at 4 ◦ C), and moisture and fat content were evaluated in left leg meat samples according to the same procedures described for M. longissimus dorsi. Furthermore, from each of the right leg meat samples, subcutaneous fat tissue was excised and homogenized, and the chemical fat was extracted with petroleum ether overnight and continually shaken in a cold water bath. Then, 2.5 g of the extracted fat were taken for the evaluation of lipid oxidation stability using the Rancimat 743 apparatus (Metrohm, Herisau, Switzerland) at 120 ◦ C and under an airflow of 20 l/min. The induction time of the samples, also known as the Rancimat Stability Index (R.S.I.), was expressed in hours. The meat from the right legs (without subcutaneous fat) was used to assess the changes in colour and fat oxidation (thiobarbituric acid reactive substances; TBARS) during storage at refrigeration temperature (2 ± 1 ◦ C). The central part of each leg was obtained by removing the upper and lower ends.

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The upper end was separated by cutting at approximately 4 cm below the end point and the lower end by cutting 4 cm above the kneecap. Then, the central part was divided into slices (2 cm thick), which were placed individually in Styrofoam trays covered by an oxygen-permeable PVC film (14,000 ml/(m2 24 h)) and stored in darkness at 3 ◦ C for a period of 21 days. The correspondent colour and TBARS analyses were then performed. Colour was measured in three different locations (M. semimembranosus, M. biceps femoris, and M. adductor) on the top cut muscular surfaces of the slices after 1, 7, 14, and 21 days of storage in CIE L*a*b* space with the same equipment and conditions previously described. Additionally, TBARS concentrations in homogenates of the muscular part of leg meat slices were evaluated at days 1 and 21, following the procedures described by Nam and Ahn (2003). Vitamin content (A and E) was determined in the left leg meat homogenates following the same methodology described for M. longissimus dorsi. Finally, the same homogenate was used for volatile extraction using a Likens–Nickerson simultaneous distillation–extraction apparatus (J&W Scientific, Folsom, CA, USA; 4-h reflux time). One flask contained 100 g of meat and 100 ml of ultrafiltered water (Millipore purification system; Mili-Q, Waters), and the other flask contained 60 ml of a spectroscopy grade diethylether (Merck, Darmstadt, Germany) as the extraction solvent. The ether solution was concentrated by distilling it in a Kuderna–Danish concentrator (Sigma–Aldrich) in a 50 ◦ C water bath until 1 ml of solution was obtained. Volatiles were separated and identified by GC–MS with a Hewlett Packard-6890 Series GC system and Hewlett Packard-5973 Inert MSD Mass Selective Detector (Agilent Technologies, Hewlett–Packard, Palo Alto, CA, USA) equipped with a HP-5 MS capillary column (30 m × 0.25 mm × 0.25 ␮m; Agilent Technologies) and using He at a flow rate of 1 ml/min as the carrier gas. Four microliters of the solution was injected (injector temperature: 230 ◦ C and split mode 50:1). Initial oven temperature was 50 ◦ C, which was increased to 95 ◦ C at a rate of 10 ◦ C/min, and then to 270 ◦ C at a rate of 10 ◦ C/min. The MS detector was activated after 6 min of injection. Ionisation energy of the mass spectrometer was −70 eV, ionisation current was 34.6 ␮A, source temperature was 200 ◦ C, scan range was 40–550 mass-to-charge ratio, and scan time was 4 s−1 . Volatile compounds were tentatively identified by comparing their mass spectra with those contained in a database (Willey 275) and their Kovacs’ Index with those from the literature whenever available. In addition, the spectrum of unidentified compounds was studied to detect the presence of sulphur, which was indicated by its characteristic isotope pattern. Concentrations of volatile compounds were expressed as area percentages. 2.4. Vitamin content of ewe’s milk and milk replacer For analysis of vitamins A and E in ewe milk and in the milk replacer, fat was first extracted from each sample (Bligh and Dyer, 1959). Vitamins were then determined as previously described for M. longissimus dorsi and left leg meat.

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2.5. Sensory analysis Triangle tests were performed by an untrained panel comprising staff members of three regional sheep breeders’ associations. Analyses were carried out with the M. longissimus dorsi portions from the lumbar region between the first and sixth lumbar vertebrae, from both sides of the carcasses. Prior to the analysis, the M. longissimus dorsi lumbar regions were deboned and then frozen at −40 ◦ C for between 3 and 9 months. Afterward, samples were thawed for 48 h at 4 ◦ C and 1-cm thick slices were broiled (without the addition of salt) in a double-sided griddle, and heated at 165 ◦ C until they reached a core temperature of 71 ◦ C; this method followed the research guidelines for cooking procedures of AMSA (1995). Three coded broiled pieces of meat were given to 33 panellists; two samples came from one rearing system, and the other sample was from the other rearing system. Each panellist was asked to identify the sample that did not match the other two. Physical facilities and sample preparation followed the recommendations described by Poste et al. (1991). 2.6. Statistics Significant differences were found by performing one-way analysis of variance (ANOVA), using STATISTICA for Windows (StatSoft Inc., 2001), to evaluate the effect of the rearing system on the physico-chemical characteristics of the suckling lamb meat and fat. Additionally, a binomial distribution was used for the results of the sensory analysis (triangle test).

3. Results and discussion 3.1. Technological meat quality traits Results of the quality traits of M. longissimus dorsi and leg meat for both rearing systems are presented in Table 1. The pH of M. longissimus dorsi was close to 5.6 for both MM and MR samples (Table 1). Other authors also found no effect of rearing lambs with either MM or MR on meat pH (Lanza et al., 2006; Napolitano et al., 2006). Additionally, no significant differences were found for moisture and fat contents in M. longissimus dorsi and leg meat (Table 1). These results differ from findings by Lanza et al. (2006), who found M. longissimus dorsi samples from MR-fed suckling lambs to be fatter than those from MM-fed lambs. This discrepancy, however, might be at least partially explained by the expected (although usually low) effect of carcass weight on fatness (Migu´elez et al., 2006). WHC (expressible juice and cooking loss) of M. longissimus dorsi seemed not to be influenced by the rearing system (Table 1); this result was also obtained by Vicenti et al. (2004). Similarly, although a higher shear

force (WBSF) was found in cooked M. longissimus dorsi samples from MM-fed animals, the rearing system used did not result in significant differences in this trait. Our results confirm findings by Napolitano et al. (2006), who also reported similar WBSF between meats from MMand MR-reared lambs. Muscle (M. longissimus dorsi) from suckling lambs fed MM showed higher L*, lower a* and higher b* values (P < 0.05) than those fed MR (Table 1). Findings regarding L* and a* values were in agreement with results obtained by Lanza et al. (2006). These authors attributed the rearing-system-related L* and a* differences to the fact that longissimus dorsi muscle from the MR group had more IMF and probably higher myoglobin content than the MM group muscle samples. In this study, however, both groups showed no significant differences for either IMF or myoglobin content, although the MR group samples showed a tendency to have higher myoglobin content. In turn, a* differences would have accounted for the L* differences given that L* values have been shown to be inversely correlated with a* values, according to Vergara et al. (1999) and to this study (data not shown). By contrast, the effect of milk source on suckling lamb meat colour has not always been detected. Napolitano et al. (2006) found no effect of rearing lambs with MM or MR on colour parameters of M. semitendinosus. Results from the present study also showed that KKCF colour parameters were comparable between animals reared on MM and those reared on MR: L*, 72.4 and 73.8; a*, 4.8 and 4.7; and b* 10.3 and 10.2, respectively (data not shown in tables). Retinol and ␦-, ␥-, and ␣-tocopherol concentrations for the MM and MR groups in M. longissimus dorsi and leg meat are shown in Table 1. Retinol and ␦-, ␥-, and ␣-tocopherol levels in the meat were dramatically influenced by the rearing system (P < 0.001). Differences in tocopherol and retinol levels in the meat could be mostly attributed to a higher amount of those vitamins (especially ␥- and ␣-tocopherol) in the MR than in the MM because retinol and tocopherols are added as ingredients in the MR. Means (±standard deviation; expressed as ␮g/100 g of dry extract) of retinol and ␦-, ␥- and ␣tocopherol content in MR were 1072 (±10), 54 (±3), 1818 (±26) and 5925 (±40) and in MM were 765 (±17), 40 (±5), 32 (±6), and 578 (±16), respectively. Lipid-oxidative stability revealed significant differences in induction time in the Rancimat test (P < 0.001) and TBARS changes (P < 0.05) during storage, with a higher stability evident for MR group samples (Table 1). Lipid-oxidative stability of meat depends on an antioxidative and pro-oxidative balance, with vitamin E content and fatty acid composition being two primary factors

M.T. Osorio et al. / Small Ruminant Research 78 (2008) 1–12

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Table 1 Quality traits of M. longissimus dorsi and leg meat (mean ± standard deviation) for different rearing systems Rearing system

Significance

Maternal milk (n = 10)

Milk replacer (n = 10)

M. longissimus dorsi pH Moisture (%) Intramuscular fat (%) Expressible juice (%) Cooking loss (%) WBSF (N) L* value a* value b* value Myoglobin (mg/g) Retinol (␮g/100 g) ␦-Tocopherol (␮g/100 g) ␥-Tocopherol (␮g/100 g) ␣-Tocopherol (␮g/100 g)

5.65 ± 0.05 75.15 ± 1.08 1.82 ± 0.28 24.81 ± 1.65 22.45 ± 1.83 45.57 ± 12.52 48.48 ± 1.11 6.78 ± 0.74 6.28 ± 0.45 2.45 ± 0.39 5.2 ± 3.4 ND 3.4 ± 3.2 100.3 ± 21.4

5.61 75.70 1.88 23.04 22.79 42.50 46.65 7.69 5.67 2.85 12.8 8.7 174.6 254.3

± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.06 0.85 0.34 2.99 1.37 12.18 0.84 0.89 0.39 0.46 2.9 2.9 61.8 48.9

NS NS NS NS NS NS

Leg meat Moisture (%) Fat (%) Retinol (␮g/100 g) ␦-Tocopherol (␮g/100 g) ␥-Tocopherol (␮g/100 g) ␣-Tocopherol (␮g/100 g) Induction timea (h) Change in TBARSb (mg MDA/kg)

68.19 ± 3.09 10.44 ± 2.21 10.38 ± 6.91 ND 4.6 ± 4.2 81.8 ± 32.4 1.54 ± 0.65 0.84 ± 0.55

71.29 10.40 43.69 15.4 147.1 224.9 6.75 0.28

± ± ± ± ± ± ± ±

2.91 3.93 18.41 4.7 46.8 77.2 2.04 0.23

NS NS

** * *

NS ***

– *** ***

***

– *** *** *** *

WBSF: Warner–Braztler shear force. ND: not detected. NS: not significant. a The induction time was determined in the subcutaneous fat from the leg. b The change in TBARS values were calculated as the difference in TBARS between measurements on day 21 and 1 under chilled storage. * P < 0.05. ** P < 0.01. *** P < 0.001.

(Morrisey et al., 1998). On the one hand, resistance to lipid oxidation is clearly enhanced by increasing levels of vitamin E in meat (Wulf et al., 1995; Macit et al., 2003; Lauzurica et al., 2005). On the other hand, the degree of unsaturation of meat fatty acids has been directly correlated with lipid oxidation rate (Morrisey et al., 1998). These two reasons may be why MM meat is more prone to oxidation than MR meat. First, MM samples had comparatively lower levels of vitamin E (Table 1). Additionally, as observed in a previous study (Osorio et al., 2007c), percentages of polyunsaturated fatty acids (PUFA) and, more specifically, those with three or more double bonds, were higher for MM than for MR meat samples (percentages of total PUFA and PUFA with three or more double bonds in IMF for MM samples were 19.6 and 9.0, whereas percentages for MR samples were 16.3 and 4.0.). As for colour changes during chilled storage (Fig. 1a), the L* value of leg meat increased during the first week. The L* value for MM samples was similar at 7, 14, and

21 days, whereas the L* value for MR samples decreased slightly with advancing time. The L* value was different (P < 0.05) between MM and MR samples at 21 days. In contrast, the value of a* tended to decline with advancing time (i.e., the meat became less red), with the most pronounced decrease during the first week (Fig. 1b). The reduction in values of a* during meat storage has been associated with an increasing percentage of metmyoglobin (Kannan et al., 2001). Differences between treatments in a* might be related to vitamin E content of the samples. The protective effect of vitamin E on lamb meat colour deterioration has been previously reported (Macit et al., 2003; Lauzurica et al., 2005), and a hindering effect of vitamin E on the oxidation of oxymyoglobin to metmyoglobin was suggested (Wulf et al., 1995). Additionally, the value of b* generally increased slightly during chilled storage for both treatments (Fig. 1c), although the change was more pronounced for MM samples. In concurrence with this observation, an increase in b* values for lamb meat stored in an 80% CO2 and 20%

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3.2. Volatile compounds of suckling lamb meat

Fig. 1. (a–c) Effect of the rearing system (MM: maternal milk; MR: milk replacer) on the changes in L*, a*; and b* values of suckling lamb meat during a 21-day period of chilled storage. Error bars represent the mean ± standard deviation (n = 10). Mean values for the same day with a star (*) represent significant differences (P < 0.05).

O2 atmosphere was reported by Berruga et al. (2005). Oxidation of myoglobin might also be responsible for changes in b*, as suggested by Jeremiah (2001). Finally, the fact that samples with lower lipid-oxidative stability (MM) were less stable to discolouration than those with higher oxidative stability (MR) agrees with the reports of Monahan et al. (1994), Kannan et al. (2001), and O’Sullivan et al. (2002).

A total of 71 volatile compounds were classified according to their chemical nature (Table 2 ) as hydrocarbons (4), aldehydes (15), ketones (4), alcohols (5), acids (9), esters (7), lactones (6), phenolic and benzene compounds (9), and sulphur-containing compounds (12). In addition, there were four unknown compounds. The predominant compounds in the volatile fraction of boiled suckling lamb meat were typical lipid-derived volatiles generated either by non-oxidative thermal degradation through hydrolysis, decarboxylation, and dehydration (Nawar, 1969) or by oxidation (Chen and Ho, 1998). Compounds attributed to non-oxidative lipid thermal degradation mainly belonged to free fatty acid, ester, alcohol, aldehyde, methylketone, and hydrocarbon nalkyl series from at least C10 to up to C20. Variability in the concentrations of these compounds between meats from MM and MR groups was related to variability in their respective fatty acid profile. A previous study (Osorio et al., 2007c) found that percentages of decanoic, pentadecanoic, hexadecanoic, and octadecanoic acids were higher in fat from MM than MR-reared lambs. Consequently, in the current experiment, volatiles probably originated from thermal degradation of those fatty acids, such as decanoic, pentadecanoic, and hexadecanoic free acids or their methyl or ethyl esters, pentadecanal, 1hexadecanol, hexadecanal, octadecanal, and octadecane, were more abundant for MM than for MR lambs. Conversely, a higher percentage of dodecanoic acid was found in fat from MR lambs (Osorio et al., 2007c), and thus, concentrations of dodecanoic free acid, ethyl dodecanoate, 1-dodecanol, and 2-tridecanone were greater for MR than for MM meat samples. Significant differences between groups were detected for some of the volatiles mentioned above. Volatiles that are reported to be typically derived from lipid oxidation (Mottram and Edwards, 1983; Mottram, 1998; Elmore et al., 2000) were more abundant in MM than MR samples. This result might be due to the lower oxidative stability of the meat from the first group (MM), which was previously observed by TBARS and the Rancimat test. In this regard, substantial differences, some significant, between meat groups were found for heptanal, 2-decenal, 2,4-decadienal, octanal, nonanal, 1-octen-3-ol, and 1-octanol percentages. These lipid oxidation-derived products seemed to some extent to be desirable compounds for the aroma of cooked meat (Reineccius, 1994). Some sulphur-containing compounds, most of them undetermined, were found in the volatile extracts, but there were no significant treatment differences. These

Table 2 Volatile compounds obtained from suckling lamb leg meat, with lambs being fed either on maternal milk or milk replacer LKTa

OKIb

Compound (when unknown or undetermined, m/zc of major fragments are given)

Reliabilityd

Maternal milk n

1600 1800 1853

1409 1599 1798 1846

Hidrocarbons Terpene, C15 H24 Hexadecane Octadecane 3,7,11,15-Tetramethylhexadecene (1-phytene)

MS MS, KI MS, KI MS, KI

Total

1260 1318 1613 1613 1817 1913 1993 2027

903 1004 1061 1104 1163 1208 1268 1319 1613 1780 1818 1919 1997 2004 2022

Aliphatic aldehydes Heptanal Octanal 2-Octenal Nonanal 2-Nonenal Decanal + 1,4-dimethyltetrasulphide 2-Decenal 2,4-Decadienal Tetradecanal Pentadecanal Hexadecanal Octadecenal (undifferentiated isomer) 9-Octadecenal (Z) Octadecenal (undifferentiated isomer) Octadecanal

MS, KI MS, KI MS, KI MS, KI MS, KI MS MS, KI MS, KI MS, KI MS MS, KI MS, KI MS + KI MS MS + KI

Total

1294 1496 1700 1910

1296 1498 1696 1902

Aliphatic ketones 2-Undecanone 2-Tridecanone 2-Pentadecanone 2-Heptadecanone

MS, KI MS, KI MS, KI MS, KI

Total

980 1075 1475 1886 1886

982 1076 1476 1677 1882

Aliphatic alcohols 1-Octen-3-ol 1-Octanol 1-Dodecanol 1-Tetradecanol 1-Hexadecanol

MS, KI MS, KI MS, KI MS MS, KI

10 10 3 10

0.29 0.29 1.43 0.31

10

1.35

10 10 3 10 5 10 10 7 10 8 10 5 10 8 6

0.29 0.21 0.13 0.74 0.18 0.15 0.20 0.20 0.52 1.00 25.64 1.16 2.42 1.08 3.72

10

35.00

10 10 10 10

0.28 2.63 3.37 2.18

10

12.16

5 4 10 10 10

0.22 0.05 0.26 0.44 0.70

Range

n

0.09–1.04 0.06–0.79 0.82–2.18 0.08–0.60

10 10 1 10

0.37 0.42 0.40 0.65

10

1.47

6 8 0 10 0 10 4 1 10 0 10 1 10 5 1

0.10 0.11 – 0.44 – 0.22 0.10 0.10 0.79 – 17.67 0.40 0.67 1.04 3.30

10

20.42

10 10 10 10

0.11 9.77 6.69 3.53

10

27.48

1 0 10 10 10

0.10 – 0.35 0.69 0.50

0.06–0.75 0.02–0.53 0.06–0.20 0.19–1.51 0.08–0.38 0.06–0.43 0.05–0.54 0.05–0.47 0.21–0.82 0.04–1.98 3.51–29.00 0.40–2.33 0.33–7.21 0.38–2.94 0.46–12.43

0.06–0.65 0.34–6.43 0.56–7.13 0.89–4.38

0.06–0.58 0.05–0.07 0.05–0.76 0.13–1.41 0.26–1.68

%

Significance Range 0.17–0.58 0.17–0.74 – 0.33–1.28

NS NS – NS NS

0.04–0.13 0.05–0.18 – 0.21–0.55 – 0.08–0.30 0.08–0.11 – 0.57–1.72 – 2.43–43.01 – 0.09–2.70 0.53–2.43 –

*

NS – NS – NS *

– *

– NS – NS NS – NS

0.06–0.18 4.12–17.16 3.22–10.05 1.96–4.84

M.T. Osorio et al. / Small Ruminant Research 78 (2008) 1–12

897/905 1004 1045/1062 1103 1160

%

Milk replacer

NS *** * * **

– – 0.17–0.62 0.39–1.05 0.30–1.13

– – NS NS NS 7

8

Table 2 (Continued ) LKTa

OKIb

Compound (when unknown or undetermined, m/zc of major fragments are given)

Reliabilityd

Maternal milk n

Total

1278 1372 1467 1572 1764 1857 1963 2145 2163

Aliphatic acids Nonanoic acid Decanoic acid Undecanoic acid Dodecanoic acid Tetradecanoic acid Pentadecanoic acid Hexadecanoic acid 9-Octadecenoic acid Octadecanoic acid

MS, KI MS, KI MS, KI MS, KI MS, KI MS, KI MS + KI MS + KI MS

Total

1589 1798 1916 2082

1595 1793 1926 1993 2100 2129 2192

Aliphatic esters Ethyl dodecanoate Ethyl tetradecanoate Methyl hexadecanoate Ethyl hexadecanoate Methyl octadecenoate Methyl octadecanoate Methyl 9,12-octadecadienoate

MS, KI MS, KI MS, KI MS MS, KI MS MS

Total

1366 1473 1660 1714 1922

1367 1473 1662 1714 1932 2110

Lactones ␥-Nonalactone ␥-Decalactone 6-␥-Dodecenolactone ␦-Dodecalactone g-Undecalactone Undetermined lactone

MS, KI MS, KI MS, KI MS, KI MS, KI MS

Total

947/963 980 1171

958 986 1161 1464 1518

Phenolic/Benzene compounds Benzaldehyde Phenol Ethylbenzaldehyde Pentylbenzaldeyde Butylated hydroxy toluene (BHT)

MS, KI MS, KI MS, KI MS MS

10

1.57

0 10 3 10 10 6 10 10 10

– 1.56 0.13 4.61 14.68 0.68 8.32 2.75 1.37

10

35.57

7 7 10 9 6 7 4

0.20 0.49 1.86 0.62 1.85 1.30 0.13

10

4.98

10 5 3 10 10 9

0.24 0.10 0.13 1.18 1.00 0.39

10

1.93

0 0 4 9 0

– – 0.08 0.19 –

Range

– 0.13–0.46 0.08–0.20 0.94–10.37 2.06–36.88 0.11–1.13 2.02–18.88 0.93–9.51 0.36–3.02

0.05–0.34 0.31–1.04 0.19–14.57 0.31–1.11 0.05–8.21 0.02–6.25 0.08–0.17

0.05–0.71 0.04–0.27 0.02–0.21 0.49–1.88 0.41–1.90 0.10–1.38

– – 0.04–0.13 0.06–0.48 –

n

%

10

1.56

4 10 0 10 10 0 10 10 10

0.08 0.39 – 14.15 11.46 – 5.22 2.09 0.97

10

35.97

10 6 10 6 10 10 0

0.74 0.25 1.27 0.32 0.84 0.77 –

10

3.90

10 0 0 10 10 2

0.13 – – 1.08 1.01 0.25

10

1.23

7 3 0 5 10

0.13 0.33 – 0.08 0.65

Significance Range NS

0.05–0.11 0.15–0.74 – 4.44–23.51 4.09–17.53 – 2.45–8.05 0.97–2.48 0.81–1.95

– *

– **

NS – NS NS NS NS

0.30–2.25 0.14–0.40 0.27–3.39 0.31–0.38 0.08–2.47 0.12–2.99 –

*

NS NS *

NS NS – NS

0.08–0.23 – – 0.82–1.50 0.79–1.41 0.07–0.45

NS – – NS NS NS NS

0.04–0.21 0.06–0.59 – 0.06–0.10 0.19–1.00

– – – *

–

M.T. Osorio et al. / Small Ruminant Research 78 (2008) 1–12

1274 1373 1463 1566 1760 1839 1963 2144

%

Milk replacer

1303 1387

1875 1969 1293 1387

Diisobutylphthalate Dibutylphthalate Indole 3-Methylindole (skatol)

MS MS MS, KI MS, KI

0.89 2.42 – 0.10

10

2.58

MS, KI MS MS MS MS

1 10 5 10 5

0.20 1.41 0.18 0.15 0.30

MS MS, KI MS MS MS MS MS

3 10 10 10 10 4 5

0.30 0.31 3.46 2.30 1.34 0.70 0.56

10

9.90

0 5 5 3

– 0.26 0.24 0.27

10

0.63

Total

970/979

1393

962 1196 1199 1208 1379 1380 1397 1687 1747 1945 2026 2031

Sulphur compounds Dimethyltrisulphide Undetermined (44, 60, 59, 163, 45, 42) Undetermined (156, 92, 64, 60, 59, 45) 1,4-Dimethyltetrasulphide + decanal Dimethyltetrathiacyclohexane (undifferentiated isomer) Methyl-dietylditiocarbamate 4,6-Dimethyl-1,2,3,5-tetrathiacyclohexane Undetermined (156, 92, 152, 59, 64, 60) Undetermined (156, 92, 64, 59, 220, 60) Undetermined (152, 59, 92, 188, 156, 60) Undetermined (156, 221, 74, 97, 59, 64) Undetermined (111, 112, 55, 43, 97, 41) Total

864 1853 1898 2185

Unknown (45, 73, 43, 55, 72, 74) (83, 97, 55, 41, 69, 43) (57, 70, 55, 41, 83, 95) (59, 72, 41, 43, 55, 57) Total

0.14–2.16 0.46–5.36 – 0.08–0.16

10 10 3 1

1.17 2.06 0.07 0.10

10

4.09

– 0.71–2.90 0.08–0.41 0.06–0.43 0.10–0.59

4 10 6 10 10

0.08 1.15 0.22 0.22 0.24

0.02–0.13 0.55–2.12 0.10–0.47 0.08–0.30 0.10–0.60

– NS NS NS NS

0.07–0.44 0.11–0.70 0,84–8.99 0.53–4.66 0.09–3.34 0.20–1.48 0.17–1.08

3 10 10 10 10 5 3

0.13 0.28 5.25 2.40 0.88 0.54 0.83

0.08–0.17 0.12–0.47 2.42–10.19 0.24–3.47 0.64–1.25 0.29–0.42 0.18–1.65

NS NS NS NS NS NS NS

10

1.21

9 2 0 6

0.10 0.30 – 0.20

10

0.28

– 0.07–0.54 0.12–0.37 0.10–0.51

0.88–2.09 0.98–3.00 0.06–0.07 –

NS NS – – NS

NS

0.04–0.16 0.46–0.52 – 0.40–0.70

– NS – NS NS

(%) Concentration of the respective compound expressed as area percentage. (n) Number of samples, out of 10, where the respective compound was detected. (NS) Not significant. (–) The correspondent value could not be calculated. a Literature Kovats indices for a DB-5 capillary column, obtained from Kondjoyan and Berdagu´ e (1996). b Observed Kovats indices. c m/z (mass-to-charge ratios). d Reliability of identification; MS, mass spectrum tentatively identified using NIST library, concordance of mass spectra >90; KI, Kovats index in agreement with literature. * P < 0.05. ** P < 0.01. *** P < 0.001.

M.T. Osorio et al. / Small Ruminant Research 78 (2008) 1–12

10 6 0 3

9

10

M.T. Osorio et al. / Small Ruminant Research 78 (2008) 1–12

compounds are generated in meat primarily as a result of degradation of sulphur amino acids and thiamine and further reactions of the formed intermediaries with Maillard reaction products (Hofmann et al., 1996; Cerny, 2007). Nevertheless, the presence of Maillard reaction products appeared to be scarce when studying the flavour of the boiled meat (Mottram, 1985; Chen and Ho, 1998). We concur with this finding. Ruminant fat species-specific volatiles such as medium branched-chain free fatty acids, tetra- and hexalactone, and 2-3-octadione (Vasta and Priolo, 2006) were not detected in suckling lamb meat. This could be partly attributed to milk being the only feed ingested by suckling lambs before slaughter. However, a typical terpene, 1-phytene, derived from the decomposition of chlorophyll (Elmore et al., 2004; Vasta and Priolo, 2006), was found in the volatiles of suckling lamb meat, and its concentration was statistically independent of the rearing system. This terpene could be mostly incorporated in lamb tissues before birth. Feeding MM to lambs would thus not represent an important source of phytene since it was not more abundant in the volatiles of the MM samples compared to those of the MR treatment. Finally, it is important to point out that residues of butylated hidroxytoluene (BHT), which is a synthetic antioxidant added to the MR (as declared on MR label), were detected in all MR samples, whereas none of the MM samples were found to contain BHT. The presence of BHT might contribute to the higher oxidative stability of MR meat samples together with the higher concentration of vitamin E and the lower levels of polyunsaturated fatty acids. 3.3. Sensory analysis Despite the observed treatment differences in the concentration of volatile compounds in the boiled meat samples, results of the triangle test showed that broiled meat samples from the rearing system treatments could not be discriminated by panellists (P > 0.05; a total of 12 of the 33 panellists correctly identified the different samples; data not shown in tables). These results disagree with those of Napolitano et al. (2002), whose panel was able to distinguish between MM and MR meat samples in a triangle test. This discrepancy might be related to the fact that in the experiment of Napolitano et al. (2002) used grilled meat and a semi-trained panel instead of the broiled meat samples and the non-trained panel used in our experiment. To summarise, MM samples showed a paler pink colour, while MR meat samples showed higher concentrations of vitamins. In addition, MM meat samples

seemed to be more prone to metmyoglobin formation and lipid oxidation changes during chilled storage than MR meat samples, which may be attributed to differences in vitamin E levels and also to BHT residues. Finally, the main differences in flavour compounds were that volatile compounds derived by non-oxidative thermal lipid degradation were clearly related to fatty acid composition of the samples, whereas volatiles derived from lipid oxidation were more abundant in MM meat samples (more susceptible to lipid oxidation). 4. Conclusions This research has shown that feeding suckling lambs with either maternal milk (MM) or a commercial milk replacer (MR) had significant effects on different suckling lamb meat quality traits. Results clearly illustrate that differences in the composition of milk sources (MM vs. MR) used in rearing suckling lambs can be responsible for significant variation in oxidative stability of fresh suckling lamb meat during storage and display and in the volatile composition of cooked suckling lamb meat. The practical implication of these results is that use of MR containing appropriate levels of antioxidants (i.e., tocopherols) and fatty acid composition may result in lower oxidation rates in suckling lamb meat compared with meat from lambs fed MM. This difference would be particularly important regarding meat with prolonged periods of storage, especially when frozen or in a modified atmosphere-packaged chilled form. This advantage, however, is only relative because, at least in Spain, most suckling lamb meat is sold fresh and loose or packed in the traditional way, and the recommended shelf life (time from slaughter to sale) of high-quality chilled suckling lamb meat is up to 8 days. In fact, a maximum storage and display time of 8 days is prescribed in the regulations of the Protected Geographical Indication “Lechazo de Castilla y Le´on” (a European quality label; BOE, 18 November, 1997). In addition, rearing suckling lambs on MR, which has a strikingly different composition compared to MM concerning antioxidant levels and fatty acid profiles, may result in a different flavour than that expected by consumers for traditional MM-fed suckling lamb meat. Further research is needed to asses the effect of dietary vitamin E levels and fatty acid profiles on the perception of suckling lamb meat flavour. Acknowledgements This study was financially supported by the Instituto Tecnol´ogico Agrario de Castilla y Le´on (ITACyL), Consejer´ıa de Agricultura y Ganader´ıa de la Junta de

M.T. Osorio et al. / Small Ruminant Research 78 (2008) 1–12

Castilla y Le´on. The authors are grateful to the Asociaci´on Nacional de Criadores de Ganado Ovino de Raza Churra (ANCHE) for providing the suckling lamb carcasses for analysis, and to Dr. Victor Kuri for his kind language assistance. References AMSA, 1995. Research Guidelines for Cookery, Sensory Evaluation and Instrumental Tenderness Measurements of Fresh Meat. American Meat Science Association in cooperation with National Live Stock and Meat Board, Chicago, USA, pp. 1–47. AOAC, 1999. Official method 991.36 fat (crude), Chapter 39. Meat and meat products. In: Cunniff, P. (Ed.), Official Methods of Analysis of the AOAC International, vol. II, 16th ed., 5th Revision. Association of Official Analytical Chemists International Gaithersburg, USA, pp. 3–4. Berruga, M.I., Vergara, H., Gallego, L., 2005. Influence of packaging conditions on microbial and lipid oxidation in lamb meat. Small Rum. Res. 57, 257–264. Bligh, E.G., Dyer, W.J., 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911–917. BOE 11 de noviembre, 1997. Orden de 5 de noviembre de 1997 por la que se ratifica el reglamento de la Indicaci´on Geogr´afica Protegida “Lechazo de Castilla y Le´on” y de su Consejo Regulador (Order of November 5th, 1997, ratifying the Regulations of the Protected Geographic Indication “Lechazo de Castilla y Le´on” and its Supervisory Council), Bolet´ın Oficial del Estado no. 276, Madrid, Spain, pp. 33799–33808. Cerny, C., 2007. Origin of carbons in sulphur-containing aroma compounds from the Maillard reaction of xylose, cysteine and thiamine. LWT-Food Sci. Technol. 40, 1309–1315. Chen, J., Ho, C.T., 1998. The flavour of pork. In: Shahidi, F. (Ed.), Flavour of Meat, Meat Products and Seafoods. Chapman and Hall, London, UK, pp. 61–83. Colomer-Rocher, F., Morand-Fehr, P., Kirton, A.H., Delfa, R., Sierra, I., 1988. M´etodos normalizados para el estudio de los caracteres cuantitativos y cualitativos de las canales caprinas y ovinas (Standardized methodology for the measurement of quantitative and qualitative properties of lamb and goat carcasses). Cuadernos INIA, no. 17, Ministerio de Agricultura, pesca y alimentaci´on, Madrid, Spain, pp. 1–30. Elmore, J.S., Mottram, D.S., Enser, M., Wood, J.D., 2000. The effects of diet and breed on the volatile compounds of cooked lamb. Meat Sci. 55, 149–159. Elmore, J.S., Warren, H.E., Mottram, D.S., Scollan, N.D., Enser, M., Richardson, R.I., Wood, J.D., 2004. A comparison of the aroma volatiles and fatty acid compositions of grilled beef muscle from Aberdeen Angus and Holstein–Friesian steers fed diets based on silage or concentrates. Meat Sci. 68, 27–33. Fisher, A.V., De Boer, H., 1994. The EAAP standard method of sheep carcass assessment. Carcass measurements and dissection procedures. Report of the EAAP Working Group on Carcass Evaluation, in cooperation with the CIHEAM Instituto Agron´omico Mediterr´aneo of Zaragoza and the CEC Directorate General for Agriculture in Brussels. Livest. Prod. Sci. (38) 149– 159. Gorraiz, C., Beriain, M.J., Chasco, J., Iraizoz, M., 2000. Descriptive analysis of meat from young ruminants in Mediterranean systems. J. Sens. Stud. 15, 137–150.

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