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Small Ruminant Research 78 (2008) 1–12

Available online at www.sciencedirect.com

Effect of rearing system on some meat quality traits andvolatile compounds of suckling lamb meat

Marıa Teresa Osorio a, Jose Marıa Zumalacarregui 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 Leon, Spainb Department of Microbiology, Faculty of Sciences, Campus Universitario, Km 1, vıa Bucaramanga,

Edificio Simon Bolıvar, Pamplona, N. de S/der, Colombiac 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 2008Available online 19 May 2008

bstract

Twenty Churra-breed suckling lamb carcasses from two groups of animals were used in this study. One group had been rearedn maternal milk (MM), and the other had been reared on milk replacer (MR) until slaughter at 25–35 days old. The effects of theype of milk on several meat quality traits were studied. These effects included pH, colour, WHC, texture, retinol and tocopheroloncentrations, colour and lipid oxidation stability, and the volatile compounds that formed during boiling of the meat. Furthermore,sensory analysis (triangle test) was carried out. The colour of M. longissimus dorsi of MM samples showed higher L*, lower a*,

nd higher b* values than those of MR samples (P < 0.05). Retinol, �-, �- and �-tocopherol levels were all higher in the meat ofambs reared on MM (P < 0.001). Rancimat tests and TBARS analysis revealed more lipid-oxidative stability for the meat of the

R group, and the colour of meat from this group was also more stable. Likewise, volatile compounds derived from lipid oxidationere more abundant in the MM samples than in the MR group samples. The presence of volatiles attributed to non-oxidative lipid

hermal degradation also differed between the two rearing systems, with concentrations of volatiles derived from dodecanoic acideing clearly higher for the MR meat samples. Residues of butylated hidroxytoluene (BHT) were detected in MR samples but notn the samples of the MM treatment. In the triangle test, an untrained panel could not detect a significant difference between MMnd MR meat samples. The present study has demonstrated that variation in the composition of milk sources (MM vs. EM) used in

earing suckling lambs may be responsible for a significant effect in oxidative stability of fresh suckling lamb meat during storagend display and in the volatile composition of cooked suckling lamb meat. Thus, meat from MR-fed suckling lambs may becomeore stable to oxidation compared to meat from MM-fed suckling lambs. MR-reared meat may, however, have a different flavour

rom what is expected from the more traditional MM-fed suckling lamb meat.2008 Elsevier B.V. All rights reserved.

ounds;

eywords: Suckling lamb; Milk replacer; Meat quality; Volatile comp

∗ Corresponding author. Tel.: +34 987291247; fax: +34 987291284.E-mail address: jmato@unileon.es (J. Mateo).

921-4488/$ – see front matter © 2008 Elsevier B.V. All rights reserved.doi:10.1016/j.smallrumres.2008.03.015

Lipid oxidation stability; Colour deterioration

1. Introduction

In Mediterranean countries, consumers prefer meatfrom light lambs fed either milk or mainly concentratediets (Vergara et al., 1999; Sanudo et al., 2006). Amonglight lambs, suckling lambs are the lightest on the market

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and have tender and juicy meat that shows a pearly whiteto pale pink colour and that is smooth in texture with adistinctive flavour (Gorraiz et al., 2000). Suckling lambsare reared exclusively on either maternal milk (MM) ormilk replacer (MR).

Several recent studies have addressed the effect ofmilk source on suckling lamb meat quality (Napolitanoet al., 2002; Vicenti et al., 2004; Lanza et al., 2006;Napolitano et al., 2006; Osorio et al., 2007a,b,c). Inthese studies, physico-chemical characteristics of lipidfraction, 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 profilesof suckling lamb tissues, which have appeared to bestrongly affected by dietary fat composition. This effecthas been observed not only when using different milksources (MM or MR) for feeding suckling lambs but alsowhen using exclusively MM but different ewe feedingsystems (Valvo et al., 2005). In addition, differences werefound in the mineral composition and colour betweenthe meat from MM- or MR-reared lambs. In spite ofthe work reported above, how feeding suckling lambswith MM or MR will affect some other major lamb meatquality traits such as lipid oxidation, meat discoloura-tion, and flavour generation during cooking is not wellunderstood.

The current study was conducted to determine theeffect of milk type on several technological quality traitsof suckling lamb meat. Some of these traits have beenpreviously studied (e.g., pH, colour, texture, WHC), andothers have not been studied before (e.g., vitamin con-tent, volatile composition, lipid oxidation, and colourdeterioration 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 witha Churra breeders association from Castilla y Leon, Spain wereused in the experiment. Of the 20 lambs, 10 were reared on MM,and the other 10 were reared on MR until slaughter (between 25and 35 days old). Animals and carcasses were the same as thosedescribed in a previous study (Osorio et al., 2007c). Means(±standard deviations) for carcass weights of the MM and theMR 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 theleg of each half carcass was separated (Colomer-Rocher et al.,1988). Pelvic fat and bones were removed from the legs (Fisherand De Boer, 1994), and the leg meat was frozen and storedat −40 ◦C until further analysis (between 1 and 6 months).

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Moreover, longissimus dorsi muscle and kidney knob chan-nel fat (KKCF) were dissected from the leg-less carcasses.In addition, the MR and the MM used for feeding the ani-mals on the farm were sampled twice and analysed for vitamincontent.

2.2. Physico-chemical characteristics in M. longisssimusdorsi

Analyses of expressible juice, pH, haem pigment content,and moisture and fat content in the M. longissimus dorsi por-tion between the 6th and 10th ribs were carried out less than48 h after slaughter. Expressible juice was determined in trip-licate, according to the methods of Grau and Hamm (1957)from small strips (approximately 300 mg) of fresh meat cutparallel to the muscle fibres. After that, the M. longissimusdorsi portions from both halves of the carcass were homoge-nized together and pH was measured using a pH meter (Model507; Crison, Barcelona, Spain) equipped with a punctureelectrode (Model 52-32; Crison). In addition, haem pigmentcontent was determined according to the method described byHornsey (1956), and moisture and intramuscular fat (IMF) per-centages were assessed according to the ISO R-1442 (1973)and AOAC method number 991.36 (AOAC, 1999), respec-tively.

Other analyses were carried out on M. longissimus dorsiportions between the 11th and 13th ribs (also less than 48 h afterslaughter). The intact portions (right and left side) were usedfor colour determination using a CM-500 chromometer (Kon-ica Minolta, Osaka, Japan). Colour measures were taken in theCIE L*a*b* colour space (illuminant: D65; visual angle: 10◦;SCI mode; 11 mm aperture for illumination and 8 mm for mea-surement; chromometer calibrated with the white calibrationtile provided with the equipment), following the methodologydescribed 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 chro-mometer touching down directly onto each of the samples’cross-section surfaces. Next, right and left M. longissimus dorsiportions were separately wrapped in aluminium foil, placed inplastic bags, and frozen for 5 months at −40 ◦C until furtheranalysis.

After thawing (48 h at 4 ◦C), the right muscle portionswere cooked in a water bath at 75 ◦C until reaching a coretemperature of 70 ◦C, and they were then cooled for 30 minat room temperature to determine water loss (cooking loss;Honikel, 1997). Afterwards, the cooked sample portions werewrapped in an oxygen permeable polyvinyl-chloride (PVC)film (14,000 ml/(m2 24 h)) and held overnight at 4 ◦C. Subse-quently, two to three rectangular prisms (1 cm × 1 cm × 2.5 cmlong), with the long side cut parallel to muscle fibre orienta-tion were obtained manually (using 1-mm-square-size linear

graph paper and a scalpel) from each sample. Shear force wasevaluated using a texture analyzer (TA-XT2i, Texture Tech-nologies Corporation, Scarsdale, NY, USA) equipped with aWarner–Bratzler device, which operated at a cross-head speedof 100 mm/min, using a 25-kg load cell, and with the sample

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risms being sheared at right angle to the fibre axis (Honikel,997).

For the analysis of vitamins A and E, IMF was firstxtracted from each of the M. longissimus dorsi left sectionsBligh and Dyer, 1959). Vitamins were then extracted fromhe IMF following methods described by Yang et al. (1992)ith slight modifications. Duplicate IMF aliquots (0.25 g) were

aponified using 1 ml of 20% methanolic KOH at 68 ◦C for5 min, and vitamins were extracted twice with 3 ml of diethylther. The extracts were combined and washed three timesith 3 ml of water. Ether was removed under nitrogen at

oom temperature, and the residue was dissolved in 1 ml ofethanol. Separation of vitamins by HPLC was carried out

sing a Separation Module (Waters 2690; Waters Corpora-ion, Milford, MA, USA) equipped with a Photodiode ArrayWaters 996) detector and a C18 column, 250 × 3.0 mm i.d.OmniSphere 5; Varian Inc., Palo Alto, CA, USA). Chromato-raphic conditions were as described by Rodas-Mendoza etl. (2003). Elution was performed with 100% methanol asobile phase at a flow-rate of 1 ml/min, with the column

ept at 50 ◦C during analysis. Detection of �-, �-, and �-ocopherols was performed at 292 nm, and retinol was detectedt 325 nm. Chromatographic peaks were identified by compar-ng retention times and spectra (210–500 nm) of samples withhose of standards (Sigma–Aldrich Sigma–Aldrich Quımica,

adrid, Spain; standard names and reference numbers: dl--tocopherol, 47783; �-tocopherol, 47784; (+)-�-Tocopherol,7785). Quantification was assessed using calibration curvesbtained with known amounts of the standards after beingubjected to the same processing as for the IMF samples, asentioned above.

.3. Physico-chemical characteristics in kidney knobhannel fat and leg meat of suckling lambs

Fat colour was determined on the surface of an intact portionf fresh KKCF (more than 2 cm wide) before 48 h post-mortem,n the CIE L*a*b* colour space using the same chromometer,arameters and conditions previously mentioned.

Frozen leg meat samples were thawed (48 h at 4 ◦C), andoisture and fat content were evaluated in left leg meat samples

ccording to the same procedures described for M. longis-imus dorsi. Furthermore, from each of the right leg meatamples, subcutaneous fat tissue was excised and homoge-ized, and the chemical fat was extracted with petroleumther overnight and continually shaken in a cold water bath.hen, 2.5 g of the extracted fat were taken for the evaluationf lipid oxidation stability using the Rancimat 743 appara-us (Metrohm, Herisau, Switzerland) at 120 ◦C and under anirflow of 20 l/min. The induction time of the samples, alsonown as the Rancimat Stability Index (R.S.I.), was expressedn hours.

The meat from the right legs (without subcutaneous fat)as used to assess the changes in colour and fat oxidation

thiobarbituric acid reactive substances; TBARS) during stor-ge at refrigeration temperature (2 ± 1 ◦C). The central part ofach leg was obtained by removing the upper and lower ends.

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The upper end was separated by cutting at approximately 4 cmbelow the end point and the lower end by cutting 4 cm abovethe kneecap. Then, the central part was divided into slices (2 cmthick), which were placed individually in Styrofoam trays cov-ered 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 cor-respondent colour and TBARS analyses were then performed.Colour was measured in three different locations (M. semimem-branosus, M. biceps femoris, and M. adductor) on the top cutmuscular surfaces of the slices after 1, 7, 14, and 21 days ofstorage in CIE L*a*b* space with the same equipment andconditions previously described. Additionally, TBARS con-centrations in homogenates of the muscular part of leg meatslices were evaluated at days 1 and 21, following the proceduresdescribed by Nam and Ahn (2003).

Vitamin content (A and E) was determined in the left legmeat homogenates following the same methodology describedfor M. longissimus dorsi. Finally, the same homogenatewas used for volatile extraction using a Likens–Nickersonsimultaneous distillation–extraction apparatus (J&W Scien-tific, Folsom, CA, USA; 4-h reflux time). One flask contained100 g of meat and 100 ml of ultrafiltered water (Milliporepurification system; Mili-Q, Waters), and the other flask con-tained 60 ml of a spectroscopy grade diethylether (Merck,Darmstadt, Germany) as the extraction solvent. The ether solu-tion was concentrated by distilling it in a Kuderna–Danishconcentrator (Sigma–Aldrich) in a 50 ◦C water bath until 1 mlof solution was obtained. Volatiles were separated and iden-tified by GC–MS with a Hewlett Packard-6890 Series GCsystem and Hewlett Packard-5973 Inert MSD Mass Selec-tive Detector (Agilent Technologies, Hewlett–Packard, PaloAlto, CA, USA) equipped with a HP-5 MS capillary column(30 m × 0.25 mm × 0.25 �m; Agilent Technologies) and usingHe at a flow rate of 1 ml/min as the carrier gas. Four microlitersof the solution was injected (injector temperature: 230 ◦C andsplit mode 50:1). Initial oven temperature was 50 ◦C, which wasincreased to 95 ◦C at a rate of 10 ◦C/min, and then to 270 ◦C ata rate of 10 ◦C/min. The MS detector was activated after 6 minof injection. Ionisation energy of the mass spectrometer was−70 eV, ionisation current was 34.6 �A, source temperaturewas 200 ◦C, scan range was 40–550 mass-to-charge ratio, andscan time was 4 s−1. Volatile compounds were tentatively iden-tified by comparing their mass spectra with those contained in adatabase (Willey 275) and their Kovacs’ Index with those fromthe literature whenever available. In addition, the spectrum ofunidentified compounds was studied to detect the presence ofsulphur, which was indicated by its characteristic isotope pat-tern. Concentrations of volatile compounds were expressed asarea percentages.

2.4. Vitamin content of ewe’s milk and milk replacer

For analysis of vitamins A and E in ewe milk and in themilk replacer, fat was first extracted from each sample (Blighand Dyer, 1959). Vitamins were then determined as previouslydescribed for M. longissimus dorsi and left leg meat.

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2.5. Sensory analysis

Triangle tests were performed by an untrained panelcomprising staff members of three regional sheep breeders’associations. Analyses were carried out with the M. longis-simus dorsi portions from the lumbar region between the firstand sixth lumbar vertebrae, from both sides of the carcasses.Prior to the analysis, the M. longissimus dorsi lumbar regionswere deboned and then frozen at −40 ◦C for between 3 and9 months. Afterward, samples were thawed for 48 h at 4 ◦Cand 1-cm thick slices were broiled (without the addition ofsalt) in a double-sided griddle, and heated at 165 ◦C until theyreached a core temperature of 71 ◦C; this method followed theresearch guidelines for cooking procedures of AMSA (1995).Three coded broiled pieces of meat were given to 33 pan-ellists; two samples came from one rearing system, and theother sample was from the other rearing system. Each panellistwas asked to identify the sample that did not match the othertwo. Physical facilities and sample preparation followed therecommendations described by Poste et al. (1991).

2.6. Statistics

Significant differences were found by performing one-wayanalysis of variance (ANOVA), using STATISTICA for Win-dows (StatSoft Inc., 2001), to evaluate the effect of the rearingsystem on the physico-chemical characteristics of the sucklinglamb meat and fat. Additionally, a binomial distribution wasused 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 dorsiand leg meat for both rearing systems are presented inTable 1. The pH of M. longissimus dorsi was close to 5.6for both MM and MR samples (Table 1). Other authorsalso found no effect of rearing lambs with either MM orMR on meat pH (Lanza et al., 2006; Napolitano et al.,2006).

Additionally, no significant differences were foundfor moisture and fat contents in M. longissimus dorsiand leg meat (Table 1). These results differ from find-ings by Lanza et al. (2006), who found M. longissimusdorsi samples from MR-fed suckling lambs to be fatterthan those from MM-fed lambs. This discrepancy, how-ever, might be at least partially explained by the expected(although usually low) effect of carcass weight on fatness(Miguelez et al., 2006).

WHC (expressible juice and cooking loss) of M.longissimus dorsi seemed not to be influenced by therearing system (Table 1); this result was also obtained byVicenti et al. (2004). Similarly, although a higher shear

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force (WBSF) was found in cooked M. longissimus dorsisamples from MM-fed animals, the rearing system useddid not result in significant differences in this trait. Ourresults confirm findings by Napolitano et al. (2006), whoalso reported similar WBSF between meats from MM-and MR-reared lambs.

Muscle (M. longissimus dorsi) from suckling lambsfed MM showed higher L*, lower a* and higher b* values(P < 0.05) than those fed MR (Table 1). Findings regard-ing L* and a* values were in agreement with resultsobtained by Lanza et al. (2006). These authors attributedthe rearing-system-related L* and a* differences to thefact that longissimus dorsi muscle from the MR grouphad more IMF and probably higher myoglobin contentthan the MM group muscle samples. In this study, how-ever, both groups showed no significant differences foreither IMF or myoglobin content, although the MR groupsamples showed a tendency to have higher myoglobincontent. In turn, a* differences would have accounted forthe L* differences given that L* values have been shownto be inversely correlated with a* values, according toVergara et al. (1999) and to this study (data not shown).By contrast, the effect of milk source on suckling lambmeat colour has not always been detected. Napolitano etal. (2006) found no effect of rearing lambs with MM orMR on colour parameters of M. semitendinosus. Resultsfrom the present study also showed that KKCF colourparameters were comparable between animals reared onMM 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 notshown in tables).

Retinol and �-, �-, and �-tocopherol concentrationsfor the MM and MR groups in M. longissimus dorsi andleg meat are shown in Table 1. Retinol and �-, �-, and�-tocopherol levels in the meat were dramatically influ-enced by the rearing system (P < 0.001). Differences intocopherol and retinol levels in the meat could be mostlyattributed to a higher amount of those vitamins (espe-cially �- and �-tocopherol) in the MR than in the MMbecause retinol and tocopherols are added as ingredi-ents in the MR. Means (±standard deviation; expressedas �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 differ-ences 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 antiox-idative and pro-oxidative balance, with vitamin E contentand fatty acid composition being two primary factors

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Table 1Quality 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 dorsipH 5.65 ± 0.05 5.61 ± 0.06 NSMoisture (%) 75.15 ± 1.08 75.70 ± 0.85 NSIntramuscular fat (%) 1.82 ± 0.28 1.88 ± 0.34 NSExpressible juice (%) 24.81 ± 1.65 23.04 ± 2.99 NSCooking loss (%) 22.45 ± 1.83 22.79 ± 1.37 NSWBSF (N) 45.57 ± 12.52 42.50 ± 12.18 NSL* value 48.48 ± 1.11 46.65 ± 0.84 **

a* value 6.78 ± 0.74 7.69 ± 0.89 *

b* value 6.28 ± 0.45 5.67 ± 0.39 *

Myoglobin (mg/g) 2.45 ± 0.39 2.85 ± 0.46 NSRetinol (�g/100 g) 5.2 ± 3.4 12.8 ± 2.9 ***

�-Tocopherol (�g/100 g) ND 8.7 ± 2.9 –�-Tocopherol (�g/100 g) 3.4 ± 3.2 174.6 ± 61.8 ***

�-Tocopherol (�g/100 g) 100.3 ± 21.4 254.3 ± 48.9 ***

Leg meatMoisture (%) 68.19 ± 3.09 71.29 ± 2.91 NSFat (%) 10.44 ± 2.21 10.40 ± 3.93 NSRetinol (�g/100 g) 10.38 ± 6.91 43.69 ± 18.41 ***

�-Tocopherol (�g/100 g) ND 15.4 ± 4.7 –�-Tocopherol (�g/100 g) 4.6 ± 4.2 147.1 ± 46.8 ***

�-Tocopherol (�g/100 g) 81.8 ± 32.4 224.9 ± 77.2 ***

Induction timea (h) 1.54 ± 0.65 6.75 ± 2.04 ***

Change in TBARSb (mg MDA/kg) 0.84 ± 0.55 0.28 ± 0.23 *

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.

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* P < 0.05.** P < 0.01.** P < 0.001.

Morrisey et al., 1998). On the one hand, resistance toipid oxidation is clearly enhanced by increasing lev-ls of vitamin E in meat (Wulf et al., 1995; Macit etl., 2003; Lauzurica et al., 2005). On the other hand,he degree of unsaturation of meat fatty acids has beenirectly correlated with lipid oxidation rate (Morriseyt al., 1998). These two reasons may be why MM meats more prone to oxidation than MR meat. First, MMamples had comparatively lower levels of vitamin ETable 1). Additionally, as observed in a previous studyOsorio et al., 2007c), percentages of polyunsaturatedatty acids (PUFA) and, more specifically, those withhree or more double bonds, were higher for MM thanor MR meat samples (percentages of total PUFA andUFA with three or more double bonds in IMF for MMamples were 19.6 and 9.0, whereas percentages for MR

amples were 16.3 and 4.0.).

As for colour changes during chilled storage (Fig. 1a),he L* value of leg meat increased during the first week.he L* value for MM samples was similar at 7, 14, and

21 days, whereas the L* value for MR samples decreasedslightly with advancing time. The L* value was different(P < 0.05) between MM and MR samples at 21 days. Incontrast, the value of a* tended to decline with advanc-ing time (i.e., the meat became less red), with the mostpronounced decrease during the first week (Fig. 1b).The reduction in values of a* during meat storage hasbeen associated with an increasing percentage of met-myoglobin (Kannan et al., 2001). Differences betweentreatments in a* might be related to vitamin E content ofthe samples. The protective effect of vitamin E on lambmeat colour deterioration has been previously reported(Macit et al., 2003; Lauzurica et al., 2005), and a hinder-ing effect of vitamin E on the oxidation of oxymyoglobinto 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 sam-ples. In concurrence with this observation, an increase inb* values for lamb meat stored in an 80% CO2 and 20%

6 M.T. Osorio et al. / Small Ruminan

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 lambmeat during a 21-day period of chilled storage. Error bars represent

the mean ± standard deviation (n = 10). Mean values for the same daywith a star (*) represent significant differences (P < 0.05).

O2 atmosphere was reported by Berruga et al. (2005).Oxidation of myoglobin might also be responsible forchanges 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 withhigher oxidative stability (MR) agrees with the reportsof Monahan et al. (1994), Kannan et al. (2001), andO’Sullivan et al. (2002).

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3.2. Volatile compounds of suckling lamb meat

A total of 71 volatile compounds were classifiedaccording to their chemical nature (Table 2 ) as hydrocar-bons (4), aldehydes (15), ketones (4), alcohols (5), acids(9), esters (7), lactones (6), phenolic and benzene com-pounds (9), and sulphur-containing compounds (12). Inaddition, there were four unknown compounds. The pre-dominant compounds in the volatile fraction of boiledsuckling lamb meat were typical lipid-derived volatilesgenerated either by non-oxidative thermal degradationthrough hydrolysis, decarboxylation, and dehydration(Nawar, 1969) or by oxidation (Chen and Ho, 1998).

Compounds attributed to non-oxidative lipid thermaldegradation mainly belonged to free fatty acid, ester,alcohol, aldehyde, methylketone, and hydrocarbon n-alkyl series from at least C10 to up to C20. Variability inthe concentrations of these compounds between meatsfrom MM and MR groups was related to variabilityin their respective fatty acid profile. A previous study(Osorio et al., 2007c) found that percentages of decanoic,pentadecanoic, hexadecanoic, and octadecanoic acidswere higher in fat from MM than MR-reared lambs. Con-sequently, in the current experiment, volatiles probablyoriginated from thermal degradation of those fatty acids,such as decanoic, pentadecanoic, and hexadecanoic freeacids or their methyl or ethyl esters, pentadecanal, 1-hexadecanol, hexadecanal, octadecanal, and octadecane,were more abundant for MM than for MR lambs. Con-versely, a higher percentage of dodecanoic acid wasfound in fat from MR lambs (Osorio et al., 2007c), andthus, concentrations of dodecanoic free acid, ethyl dode-canoate, 1-dodecanol, and 2-tridecanone were greater forMR than for MM meat samples. Significant differencesbetween groups were detected for some of the volatilesmentioned above.

Volatiles that are reported to be typically derived fromlipid oxidation (Mottram and Edwards, 1983; Mottram,1998; Elmore et al., 2000) were more abundant inMM than MR samples. This result might be due tothe lower oxidative stability of the meat from the firstgroup (MM), which was previously observed by TBARSand the Rancimat test. In this regard, substantial dif-ferences, some significant, between meat groups werefound for heptanal, 2-decenal, 2,4-decadienal, octanal,nonanal, 1-octen-3-ol, and 1-octanol percentages. Theselipid oxidation-derived products seemed to some extentto be desirable compounds for the aroma of cooked meat

(Reineccius, 1994).

Some sulphur-containing compounds, most of themundetermined, were found in the volatile extracts, butthere were no significant treatment differences. These

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Table 2Volatile 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 Milk replacer Significance

n % Range n % Range

Hidrocarbons1409 Terpene, C15H24 MS 10 0.29 0.09–1.04 10 0.37 0.17–0.58 NS

1600 1599 Hexadecane MS, KI 10 0.29 0.06–0.79 10 0.42 0.17–0.74 NS1800 1798 Octadecane MS, KI 3 1.43 0.82–2.18 1 0.40 – –1853 1846 3,7,11,15-Tetramethylhexadecene (1-phytene) MS, KI 10 0.31 0.08–0.60 10 0.65 0.33–1.28 NS

Total 10 1.35 10 1.47 NS

Aliphatic aldehydes897/905 903 Heptanal MS, KI 10 0.29 0.06–0.75 6 0.10 0.04–0.13 *

1004 1004 Octanal MS, KI 10 0.21 0.02–0.53 8 0.11 0.05–0.18 NS1045/1062 1061 2-Octenal MS, KI 3 0.13 0.06–0.20 0 – – –1103 1104 Nonanal MS, KI 10 0.74 0.19–1.51 10 0.44 0.21–0.55 NS1160 1163 2-Nonenal MS, KI 5 0.18 0.08–0.38 0 – – –

1208 Decanal + 1,4-dimethyltetrasulphide MS 10 0.15 0.06–0.43 10 0.22 0.08–0.30 NS1260 1268 2-Decenal MS, KI 10 0.20 0.05–0.54 4 0.10 0.08–0.11 *

1318 1319 2,4-Decadienal MS, KI 7 0.20 0.05–0.47 1 0.10 – –1613 1613 Tetradecanal MS, KI 10 0.52 0.21–0.82 10 0.79 0.57–1.72 *

1613 1780 Pentadecanal MS 8 1.00 0.04–1.98 0 – – –1817 1818 Hexadecanal MS, KI 10 25.64 3.51–29.00 10 17.67 2.43–43.01 NS1913 1919 Octadecenal (undifferentiated isomer) MS, KI 5 1.16 0.40–2.33 1 0.40 – –1993 1997 9-Octadecenal (Z) MS + KI 10 2.42 0.33–7.21 10 0.67 0.09–2.70 NS

2004 Octadecenal (undifferentiated isomer) MS 8 1.08 0.38–2.94 5 1.04 0.53–2.43 NS2027 2022 Octadecanal MS + KI 6 3.72 0.46–12.43 1 3.30 – –

Total 10 35.00 10 20.42 NS

Aliphatic ketones1294 1296 2-Undecanone MS, KI 10 0.28 0.06–0.65 10 0.11 0.06–0.18 NS1496 1498 2-Tridecanone MS, KI 10 2.63 0.34–6.43 10 9.77 4.12–17.16 ***

1700 1696 2-Pentadecanone MS, KI 10 3.37 0.56–7.13 10 6.69 3.22–10.05 *

1910 1902 2-Heptadecanone MS, KI 10 2.18 0.89–4.38 10 3.53 1.96–4.84 *

Total 10 12.16 10 27.48 **

Aliphatic alcohols980 982 1-Octen-3-ol MS, KI 5 0.22 0.06–0.58 1 0.10 – –1075 1076 1-Octanol MS, KI 4 0.05 0.05–0.07 0 – – –1475 1476 1-Dodecanol MS, KI 10 0.26 0.05–0.76 10 0.35 0.17–0.62 NS1886 1677 1-Tetradecanol MS 10 0.44 0.13–1.41 10 0.69 0.39–1.05 NS1886 1882 1-Hexadecanol MS, KI 10 0.70 0.26–1.68 10 0.50 0.30–1.13 NS

8M

.T.Osorio

etal./SmallR

uminantR

esearch78

(2008)1–12

Table 2 (Continued )

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

Reliabilityd Maternal milk Milk replacer Significance

n % Range n % Range

Total 10 1.57 10 1.56 NS

Aliphatic acids1274 1278 Nonanoic acid MS, KI 0 – – 4 0.08 0.05–0.11 –1373 1372 Decanoic acid MS, KI 10 1.56 0.13–0.46 10 0.39 0.15–0.74 *

1463 1467 Undecanoic acid MS, KI 3 0.13 0.08–0.20 0 – – –1566 1572 Dodecanoic acid MS, KI 10 4.61 0.94–10.37 10 14.15 4.44–23.51 **

1760 1764 Tetradecanoic acid MS, KI 10 14.68 2.06–36.88 10 11.46 4.09–17.53 NS1839 1857 Pentadecanoic acid MS, KI 6 0.68 0.11–1.13 0 – – –1963 1963 Hexadecanoic acid MS + KI 10 8.32 2.02–18.88 10 5.22 2.45–8.05 NS2144 2145 9-Octadecenoic acid MS + KI 10 2.75 0.93–9.51 10 2.09 0.97–2.48 NS

2163 Octadecanoic acid MS 10 1.37 0.36–3.02 10 0.97 0.81–1.95 NS

Total 10 35.57 10 35.97 NS

Aliphatic esters1589 1595 Ethyl dodecanoate MS, KI 7 0.20 0.05–0.34 10 0.74 0.30–2.25 *

1798 1793 Ethyl tetradecanoate MS, KI 7 0.49 0.31–1.04 6 0.25 0.14–0.40 NS1916 1926 Methyl hexadecanoate MS, KI 10 1.86 0.19–14.57 10 1.27 0.27–3.39 NS

1993 Ethyl hexadecanoate MS 9 0.62 0.31–1.11 6 0.32 0.31–0.38 *

2082 2100 Methyl octadecenoate MS, KI 6 1.85 0.05–8.21 10 0.84 0.08–2.47 NS2129 Methyl octadecanoate MS 7 1.30 0.02–6.25 10 0.77 0.12–2.99 NS2192 Methyl 9,12-octadecadienoate MS 4 0.13 0.08–0.17 0 – – –

Total 10 4.98 10 3.90 NS

Lactones1366 1367 �-Nonalactone MS, KI 10 0.24 0.05–0.71 10 0.13 0.08–0.23 NS1473 1473 �-Decalactone MS, KI 5 0.10 0.04–0.27 0 – – –1660 1662 6-�-Dodecenolactone MS, KI 3 0.13 0.02–0.21 0 – – –1714 1714 �-Dodecalactone MS, KI 10 1.18 0.49–1.88 10 1.08 0.82–1.50 NS1922 1932 g-Undecalactone MS, KI 10 1.00 0.41–1.90 10 1.01 0.79–1.41 NS

2110 Undetermined lactone MS 9 0.39 0.10–1.38 2 0.25 0.07–0.45 NS

Total 10 1.93 10 1.23 NS

Phenolic/Benzene compounds947/963 958 Benzaldehyde MS, KI 0 – – 7 0.13 0.04–0.21 –980 986 Phenol MS, KI 0 – – 3 0.33 0.06–0.59 –1171 1161 Ethylbenzaldehyde MS, KI 4 0.08 0.04–0.13 0 – – –

1464 Pentylbenzaldeyde MS 9 0.19 0.06–0.48 5 0.08 0.06–0.10 *

1518 Butylated hydroxy toluene (BHT) MS 0 – – 10 0.65 0.19–1.00 –

M.T.O

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1–129

1875 Diisobutylphthalate MS 10 0.89 0.14–2.16 10 1.17 0.88–2.09 NS1969 Dibutylphthalate MS 6 2.42 0.46–5.36 10 2.06 0.98–3.00 NS

1303 1293 Indole MS, KI 0 – – 3 0.07 0.06–0.07 –1387 1387 3-Methylindole (skatol) MS, KI 3 0.10 0.08–0.16 1 0.10 – –

Total 10 2.58 10 4.09 NS

Sulphur compounds970/979 962 Dimethyltrisulphide MS, KI 1 0.20 – 4 0.08 0.02–0.13 –

1196 Undetermined (44, 60, 59, 163, 45, 42) MS 10 1.41 0.71–2.90 10 1.15 0.55–2.12 NS1199 Undetermined (156, 92, 64, 60, 59, 45) MS 5 0.18 0.08–0.41 6 0.22 0.10–0.47 NS1208 1,4-Dimethyltetrasulphide + decanal MS 10 0.15 0.06–0.43 10 0.22 0.08–0.30 NS1379 Dimethyltetrathiacyclohexane (undifferentiated

isomer)MS 5 0.30 0.10–0.59 10 0.24 0.10–0.60 NS

1380 Methyl-dietylditiocarbamate MS 3 0.30 0.07–0.44 3 0.13 0.08–0.17 NS1393 1397 4,6-Dimethyl-1,2,3,5-tetrathiacyclohexane MS, KI 10 0.31 0.11–0.70 10 0.28 0.12–0.47 NS

1687 Undetermined (156, 92, 152, 59, 64, 60) MS 10 3.46 0,84–8.99 10 5.25 2.42–10.19 NS1747 Undetermined (156, 92, 64, 59, 220, 60) MS 10 2.30 0.53–4.66 10 2.40 0.24–3.47 NS1945 Undetermined (152, 59, 92, 188, 156, 60) MS 10 1.34 0.09–3.34 10 0.88 0.64–1.25 NS2026 Undetermined (156, 221, 74, 97, 59, 64) MS 4 0.70 0.20–1.48 5 0.54 0.29–0.42 NS2031 Undetermined (111, 112, 55, 43, 97, 41) MS 5 0.56 0.17–1.08 3 0.83 0.18–1.65 NS

Total 10 9.90 10 1.21 NS

Unknown864 (45, 73, 43, 55, 72, 74) 0 – – 9 0.10 0.04–0.16 –

1853 (83, 97, 55, 41, 69, 43) 5 0.26 0.07–0.54 2 0.30 0.46–0.52 NS1898 (57, 70, 55, 41, 83, 95) 5 0.24 0.12–0.37 0 – – –2185 (59, 72, 41, 43, 55, 57) 3 0.27 0.10–0.51 6 0.20 0.40–0.70 NS

Total 10 0.63 10 0.28 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. (–) Thecorrespondent value could not be calculated.

a Literature Kovats indices for a DB-5 capillary column, obtained from Kondjoyan and Berdague (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.

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compounds are generated in meat primarily as a result ofdegradation of sulphur amino acids and thiamine and fur-ther reactions of the formed intermediaries with Maillardreaction products (Hofmann et al., 1996; Cerny, 2007).Nevertheless, the presence of Maillard reaction productsappeared to be scarce when studying the flavour of theboiled meat (Mottram, 1985; Chen and Ho, 1998). Weconcur with this finding.

Ruminant fat species-specific volatiles such asmedium branched-chain free fatty acids, tetra- and hex-alactone, and 2-3-octadione (Vasta and Priolo, 2006)were not detected in suckling lamb meat. This could bepartly attributed to milk being the only feed ingestedby suckling lambs before slaughter. However, a typicalterpene, 1-phytene, derived from the decomposition ofchlorophyll (Elmore et al., 2004; Vasta and Priolo, 2006),was found in the volatiles of suckling lamb meat, and itsconcentration was statistically independent of the rear-ing system. This terpene could be mostly incorporated inlamb tissues before birth. Feeding MM to lambs wouldthus not represent an important source of phytene sinceit was not more abundant in the volatiles of the MMsamples compared to those of the MR treatment.

Finally, it is important to point out that residues ofbutylated hidroxytoluene (BHT), which is a syntheticantioxidant added to the MR (as declared on MR label),were detected in all MR samples, whereas none of theMM samples were found to contain BHT. The presenceof BHT might contribute to the higher oxidative stabilityof MR meat samples together with the higher concentra-tion of vitamin E and the lower levels of polyunsaturatedfatty acids.

3.3. Sensory analysis

Despite the observed treatment differences in the con-centration of volatile compounds in the boiled meatsamples, results of the triangle test showed that broiledmeat samples from the rearing system treatments couldnot be discriminated by panellists (P > 0.05; a total of12 of the 33 panellists correctly identified the differentsamples; data not shown in tables). These results disagreewith those of Napolitano et al. (2002), whose panel wasable to distinguish between MM and MR meat samplesin a triangle test. This discrepancy might be related tothe fact that in the experiment of Napolitano et al. (2002)used grilled meat and a semi-trained panel instead of thebroiled meat samples and the non-trained panel used in

our experiment.

To summarise, MM samples showed a paler pinkcolour, while MR meat samples showed higher con-centrations of vitamins. In addition, MM meat samples

t Research 78 (2008) 1–12

seemed to be more prone to metmyoglobin formationand lipid oxidation changes during chilled storage thanMR meat samples, which may be attributed to differ-ences in vitamin E levels and also to BHT residues.Finally, the main differences in flavour compounds werethat volatile compounds derived by non-oxidative ther-mal lipid degradation were clearly related to fatty acidcomposition of the samples, whereas volatiles derivedfrom lipid oxidation were more abundant in MM meatsamples (more susceptible to lipid oxidation).

4. Conclusions

This research has shown that feeding suckling lambswith either maternal milk (MM) or a commercial milkreplacer (MR) had significant effects on different suck-ling lamb meat quality traits. Results clearly illustratethat differences in the composition of milk sources (MMvs. MR) used in rearing suckling lambs can be responsi-ble for significant variation in oxidative stability of freshsuckling lamb meat during storage and display and inthe volatile composition of cooked suckling lamb meat.The practical implication of these results is that use ofMR containing appropriate levels of antioxidants (i.e.,tocopherols) and fatty acid composition may result inlower oxidation rates in suckling lamb meat comparedwith meat from lambs fed MM. This difference wouldbe particularly important regarding meat with prolongedperiods of storage, especially when frozen or in a modi-fied atmosphere-packaged chilled form. This advantage,however, is only relative because, at least in Spain, mostsuckling lamb meat is sold fresh and loose or packed inthe traditional way, and the recommended shelf life (timefrom slaughter to sale) of high-quality chilled sucklinglamb meat is up to 8 days. In fact, a maximum storageand display time of 8 days is prescribed in the regula-tions of the Protected Geographical Indication “Lechazode Castilla y Leon” (a European quality label; BOE, 18November, 1997). In addition, rearing suckling lambson MR, which has a strikingly different compositioncompared to MM concerning antioxidant levels and fattyacid profiles, may result in a different flavour than thatexpected by consumers for traditional MM-fed sucklinglamb meat. Further research is needed to asses the effectof dietary vitamin E levels and fatty acid profiles on theperception of suckling lamb meat flavour.

Acknowledgements

This study was financially supported by the Insti-tuto Tecnologico Agrario de Castilla y Leon (ITACyL),Consejerıa de Agricultura y Ganaderıa de la Junta de

uminan

CcCcl

R

A

A

B

B

B

C

C

C

E

E

F

G

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astilla y Leon. The authors are grateful to the Aso-iacion Nacional de Criadores de Ganado Ovino de Razahurra (ANCHE) for providing the suckling lamb car-asses for analysis, and to Dr. Victor Kuri for his kindanguage assistance.

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