The restriction of grazing duration does not compromise lamb meat colour and oxidative stability

Meat Science 92 (2012) 30–35

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The restriction of grazing duration does not compromise lamb meat colour and oxidative stability G. Luciano a,⁎, L. Biondi a, R.I. Pagano a, M. Scerra b, V. Vasta a, P. López-Andrés a, B. Valenti a, M. Lanza a, A. Priolo a, M. Avondo a a b

DISPA, Sezione di Scienze delle Produzioni Animali, University of Catania, Via Valdisavoia 5, 95123, Catania, Italy Dipartimento di Scienze e Tecnologie Agro-forestali e Ambientali, University of Reggio Calabria, Località Feo di Vito, 89100, Reggio Calabria, Italy

a r t i c l e

i n f o

Article history: Received 20 December 2011 Received in revised form 18 March 2012 Accepted 31 March 2012 Keywords: Lamb meat Lipid oxidation Colour stability Diet

a b s t r a c t Over 72 days, 33 lambs were fed: concentrates in stall (S), grass at pasture for 8 hours (8 h), or grass at pasture for 4 hours in the afternoon (4 h-PM). The 4 h-PM treatment did not affect the carcass yield compared to the 8 h treatment. Meat colour development after blooming was unaffected by the treatments. The 4 h-PM treatment increased the proportion of polyunsaturated fatty acids (PUFA; P b 0.0005) and of the highly peroxidizable fatty acids (HP-PUFA; P b 0.001) in meat compared to the 8 h treatment. The S treatment increased lipid oxidation (higher TBARS values) and impaired colour stability (higher H* values) of meat over storage compared to the 8 h and 4 h-PM treatments (P b 0.0005 and P = 0.003, respectively). No difference in meat oxidative stability was found between the 8 h and the 4 h-PM treatments. In conclusion, growing lambs can tolerate a restriction of grazing duration without detrimental effects on performances and meat oxidative stability. © 2012 Elsevier Ltd. All rights reserved.

1. Introduction The oxidative deterioration of meat is a major concern for all in the production chain. Indeed, the production of unpleasant off-flavours and the deterioration of meat colour consequent to the oxidation of lipids and myoglobin, respectively, are responsible for significant product discards (McKenna et al., 2005). Meat oxidative stability depends on several factors, with one of the most important being the balance between antioxidant and pro-oxidant components in muscle (Descalzo & Sancho, 2008). The polyunsaturated fatty acids (PUFA) in the cell membranes are the preferential substrates where lipid oxidation initiates and propagates (Gray, Gomaa, & Buckley, 1996). Therefore, together with metal ions, haem proteins and reactive oxygen species, PUFA can be considered pro-oxidant components, as a high degree of unsaturation of the muscle exposes it to oxidative damage (Morrissey, Sheehy, Galvin, Kerry, & Buckley, 1998). On the other hand, endogenous antioxidant defences and exogenous antioxidant molecules of dietary origin are able to extend meat shelf life by counteracting the oxidative reactions. The diet of the animals can strongly affect both antioxidant intake and muscle fatty acid composition, with important consequences on meat oxidative stability (Wood & Enser, 1997). Compared to diets based on concentrate feeds, dietary strategies based on pasture have

⁎ Corresponding author. Tel.: + 39 095234486; fax: + 39 095234345. E-mail address: [email protected] (G. Luciano). 0309-1740/$ – see front matter © 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.meatsci.2012.03.017

been reported to enhance the concentration of PUFA in muscle and to provide high levels of antioxidants (such as vitamin E and carotenoids) with a consequent improvement of meat oxidative stability (Faustman, Sun, Mancini, & Suman, 2010). Mediterranean environments are characterized by climate conditions whereby pasture availability is often limited (Vasta, Nudda, Cannas, Lanza, & Priolo, 2008). In this context, the possibility of restricting the time spent at pasture, thus reducing grazing pressure, may be of interest, though, such strategies should not impair animals' performances and product quality. In pigs, it has been reported that feeding restrictions impaired the deposition of vitamin E in muscle and negatively affected meat lipid oxidation over storage (Mason et al., 2005). Furthermore, it has been shown that food restriction in lambs fed a concentrate-based diet consistently lowered the concentration of glutathione in muscle with a consequent reduction of the muscle's overall antioxidant status, although lipid oxidation and colour stability were not measured (Savary-Auzeloux, Durand, Gruffat, Bauchart, & Ortigues-Marty, 2008). The present study is part of a broader project aiming at studying the impact of restricting the time at pasture for growing lambs on a number of meat quality parameters. From the experiment presented here, the results on the effects of the restriction of grazing duration on intramuscular fatty acid composition and fat volatile organic compounds have already been published (Vasta et al., 2012a; 2012b). Specifically, for the first time, the effect of limiting access to pasture on meat colour and oxidative stability has been studied. To achieve this objective, meat from lambs allowed a restricted time at pasture

G. Luciano et al. / Meat Science 92 (2012) 30–35

in the afternoon was compared with that from lambs grazing for the whole day, with an expected high oxidative stability, and with that from animals raised on concentrate feeds in stall, with an expected high oxidative instability. 2. Materials and methods 2.1. Animals and diets The experiment was conducted on a farm in Southern Italy (38°42′ 24″ N and 16°00′12″) from March to mid May 2010. The experiment was carried out in accordance with the EC Directive 86/609/EEC for animal experiments. Thirty-three Merinizzata Italiana male entire lambs (average body weight: 16.0 kg± SD 2.15 kg) were blocked in groups of 3 on a descending body weight (BW) basis and, within block, assigned randomly to one of three groups. Dietary treatments included: exclusive concentrate feeding in stall (9 lambs; S group), grass at pasture for 8hour grazing (12 lambs; 8 h group) and grass at pasture for a restricted 4-h grazing in the afternoon (12 lambs; 4 h-PM group). Over 20 days, lambs were adapted to the experimental treatments. During this period, animals in the S treatment were kept indoors and the proportion of the weaning concentrate in the diet was gradually reduced by replacement with the experimental concentrate. The 24 grass-fed lambs were at pasture for the time established for each group and, once in stall, received a decreasing amount of hay until complete elimination from the diet. At 90 days of age, animals were on the respective experimental treatments for a 72-day period. The 24 pasture-fed lambs were allowed to graze on a 1 ha reygrass (Lolium perenne) sward which was divided into 6 plots, each allowed to one sub-group of 4 lambs within each treatment (i.e.: 3 plots for the 8 h group and 3 plots for the 4 h-PM group). Lambs on the 8 h treatment grazed from 9 am to 5 pm, while animals in the 4 h-PM group grazed from 1 pm to 5 pm. Every day, at the end of the time at pasture, each sub-group of 4 lambs from the same parcel was kept indoors in multiple boxes without receiving any feed supplementation, while water was always freely available. Herbage intake at pasture was estimated twice (days 15th and 65th) by equipping each lamb with a harness according to Avondo, Bordonaro, Marletta, Guastella, and D'Urso (2002). The lambs in the S treatment were individually penned for the duration of the trial and were fed a commercial barley-based concentrate, with water being always available in the pens. The concentrate contained 50 mg / kg DM of α-tocopheryl acetate and 20,000 I.U./kg of DM of vitamin A. All the animals were weighed weekly and the rations for the S group were adjusted to achieve comparable growth rates with those of the lambs in the 8 h group. 2.2. Slaughter procedures and muscle sampling At the end of the experimental period, following overnight fasting, the lambs were slaughtered at a commercial abattoir. Carcasses were weighed and halved and, within 20 min of slaughter, the longissimus dorsi (LM) was excised from the left half, vacuum-packaged and stored at 4 °C for 24 h. 2.3. Muscle final pH, colour stability and lipid oxidation measurements After 24 h of anaerobic refrigerated storage, the final pH of LM was measured using an Orion 9106 pH-meter equipped with a penetrating electrode (Orion Research Incorporated, Boston, MA). For each muscle, four 3 cm-thick slices were prepared, using one slice for each of 4 different days of storage. Muscle slices were placed in polystyrene trays, overwrapped with an oxygen permeable PVC film and stored at 4 °C. A Minolta CM 2022 colour-meter (d/8° geometry; Minolta Co. Ltd. Osaka, Japan) was used to measure L* (lightness), a* (redness), C* (saturation) and H* (hue angle) in the CIELab colour space. Measurements were made after 2 h of blooming (day 0) and, subsequently, after 3, 7 and 10 days of storage. Diffuse reflection was measured in the SCE

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(Specular Component Excluded) mode, using illuminant A and 10° standard observer. At the same days of storage as the colour measurements, lipid oxidation was measured according to Siu and Draper (1978) with minor modifications. Briefly, muscle was finely minced using a knife and 2.5 g of minced LM were homogenized with 12.5 ml of distilled water using a Heidolph Diax 900 tissue homogenizer (Heidolph Elektro GmbH & Co. KG, Kelheim, Germany) at 9500 rpm. Samples were maintained in a water/ice bath during homogenization. Then, 12.5 ml of 10% (w/v) trichloroacetic acid was added to precipitate proteins and samples were vigorously vortexed. Homogenates were filtered through Whatman No. 1 filter paper. In 15-ml Pyrex tubes, 4 ml of clear filtrate was mixed with 1 ml of 0.06 M aqueous thiobarbituric acid and samples were incubated in a water bath at 80 °C for 90 min. The absorbance of the samples at 532 nm was measured using a double beam spectrophotometer (model UV-1601; Shimadzu Corporation, Milan, Italy). The assay was calibrated using solutions of known concentrations of TEP (1,1,3,3,-tetra-ethoxypropane) in distilled water ranging from 5 to 65 nmol/4 ml. Results were expressed as mg of malonaldehyde (MDA)/kg of meat. 2.4. Muscle fatty acid composition Fatty acid analysis of the intramuscular fat from the same animals was described by Vasta et al. (2012a). Briefly, 5 g of minced LM was used to extract intramuscular fat (IMF) according to Folch, Lees, and Stanley (1957). Gas chromatographic analysis was performed with a Varian model Star 3400 CX instrument equipped with a CP 88 capillary column (length 100 m, internal diameter 0.25 mm, and film thickness 0.25 ml; Sigma). Retention times and area of each peak were computed using the Varian Star 3.4.1 software. The individual fatty acid peaks were identified by comparison of retention times with those of known mixtures of standard fatty acids (37 component FAME mix, 18919-1 AMP, Supelco, Bellefonte, PA). The concentration of PUFA was calculated as the sum of all the identified PUFA expressed as g/100 g of IMF. The concentration of the highly peroxidizable PUFA (HP-PUFA) was calculated as the sum of all the identified PUFA with three or more unsaturated bonds (Yang, Lanari, Brewster, & Tume, 2002) expressed as g/100 g of IMF. 2.5. Statistical analysis A GLM procedure was adopted to test the effect of the dietary treatment (Diet; S, 8 h and 4 h-PM) on animal performances (final body weight, average daily gain and carcass weight), on muscle ultimate pH and colour after 2 h of blooming (L*, a* and C* values) and on IMF content and fatty acid composition of LM. Tukey's test was used for comparing mean values. Data of lipid oxidation (TBARS) and colour stability parameters (a* and H* values) over storage were analysed with a repeated measures design. The model included the Diet, the time of storage (Time; days 0, 3, 7 and 10) and their interaction (Diet × Time) as fixed factors, while individual lamb was included as a random factor. Tukey's test was used for comparing mean values. All statistical analyses were performed using the software Minitab (version 14, 1995). 3. Results and discussion 3.1. Lamb growth performances As shown in Table 1, lambs allowed to graze for 8 h reached a higher live weight at slaughter compared to animals in both the S and 4 h-PM treatments (P = 0.02 and P = 0.002, respectively). However, the carcass weight of the lambs fed concentrates in stall (S group) was similar to that reached by the 8 h lambs and was higher compared to that of the 4 h-PM group (P = 0.008). Furthermore,

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G. Luciano et al. / Meat Science 92 (2012) 30–35

Table 1 Effect of the dietary treatment on animal performances. Item

Dietary treatment

Treatments 1 No. of lambs Initial BW2 (kg) Final BW 2 (kg) Carcass weight (kg) Carcass yield (%)

S 9 15.93 19.01a 8.35b 46.78b

8h 12 16.02 20.56b 7.65ab 41.21a

SEM 4 h-PM 12 16.03 18.58a 6.72a 40.33a

0.37 0.47 0.22 0.57

3

P value

NS 4 0.002 0.01 b0.0005

a, b

: within a row, means without a common superscript differ (P ≤ 0.05). Treatments were: S = lambs fed exclusively concentrates in stall; 8 h = lambs fed exclusively at pasture for 8 h (from 9 am to 5 pm); 4 h-PM = lambs fed exclusively at pasture for 4 h in the afternoon (from 1 pm to 5 pm). 2 BW: body weight. 3 SEM: standard error of the means. 4 NS: not significant (P > 0.05). 1

feeding lamb concentrates (S) resulted in the highest carcass yield compared to both 8 h and 4 h-PM treatments (P b 0.0005), despite the fact that the live weight at slaughter of animals from the S group was similar to that of the lambs in the 4 h-PM group and was lower than that of the 8 h lambs. This result could be partially explained by a lower development of the gastrointestinal tract and by higher carcass fatness in the lambs fed exclusively concentrates compared to those fed exclusively herbage at pasture (Priolo, Micol, Agabriel, Parche, & Dransfield, 2002). It is noteworthy that, despite the lower live weight, lambs that grazed for a restricted time (4 h-PM group) had similar carcass weight and carcass yield compared to those in the 8 h group. These results showed that an important restriction of grazing duration did not compromise performances of growing lambs. Perez-Ramirez, Delagarde, and Delaby (2008) compared cows allowed to graze for 4 h with animals grazing 8 h and demonstrated that a restriction of the time at pasture induces modifications of the grazing behaviour with increased proportion of the time spent grazing and of the herbage intake rate. The authors hypothesized that this adaptation could have been responsible for the minimal reduction in intake and performance in response to the restriction of the time at pasture. In the present experiment, reducing the time at pasture for the 4 h-PM group by 50% of that allowed to the 8 h group resulted in a reduction of the dry matter intake by 22.68% (485 vs 375 g/d for 8 h and 4 h-PM, respectively; P b 0.0005. Data not shown). This result, together with a possible lower physical activity of the 4 h-PM lambs compared to the 8 h group, might help explain the lack of difference in carcass weight and carcass yield between the animals in the 8 h and 4 h-PM treatments. 3.2. Muscle ultimate pH and colour parameters As shown in Table 2, muscle ultimate pH measured after 24 h of anaerobic refrigerated storage was lower in the LM from lambs in the 8 h treatment compared to that in muscle from animals in the 4 h-PM treatment (P=0.004), while intermediate values were measured in the LM from lambs fed concentrates only. Meat from animals raised on pasture has been often reported to have higher ultimate pH values compared to that from animals given concentrates only and this is attributed to the lower feeding levels or to the higher energy expenditures associated with a pasture-based feeding system, which results in a lower glycogen content in muscle (Young, Daly, Graafhuis, & Moorhead, 1997). In the present study, ultimate pH values in muscle from animals in both the S and the 8 h groups were on average 5.67, which shows a regular trend of the post mortem glycolysis in muscle and confirms that differences in muscle final pH between concentrate or pasture-fed animals do not occur when both feeding systems provide adequate feeding levels (Priolo, Micol, & Agabriel, 2001). The higher pH values found in LM from animals in the 4 h-PM treatment compared to that from lambs in the 8 h group might be partially explained by a lower feeding level of

Table 2 Effect of the dietary treatment on muscle physical characteristics, fat content and prooxidant fatty acids. Item

Dietary treatment

Treatments 1 No. of lambs Ultimate pH 2 Lightness (L*) Redness (a*) Saturation (C*) Total IMF 3 (mg/100 g LM) PUFA 4 (% of total IMF) HP-PUFA 5 (% of total IMF)

S 9 5.73ab 42.18 12.52 15.27 2011.47b 31.20b 13.37a

8h 12 5.61a 42.76 12.96 15.96 1231.50a 27.41a 14.92b

SEM 4 h-PM 12 5.97b 42.77 11.63 14.58 1087.54a 30.29b 16.83c

6

0.05 0.62 0.40 0.52 84.60 0.36 0.28

P value

0.005 NS 7 NS 7 NS 7 b 0.0005 b 0.0005 b 0.0005

a,b,c

: within a row, means without a common superscript differ (P b 0.05). Treatments were: S = lambs fed exclusively concentrates in stall; 8 h = lambs fed exclusively at pasture for 8 h (from 9 am to 5 pm); 4 h-PM = lambs fed exclusively at pasture for 4 h in the afternoon (from 1 pm to 5 pm). 2 Measured on muscle longissimus dorsi after 24 h of anaerobic storage at 4 °C. 3 IMF: intramuscular fat. 4 PUFA: polyunsaturated fatty acids; calculated as the sum of: C18:2 trans-9, trans12; C18:2 cis-9, cis-12; C18:3 cis-6, cis-9, cis-12; C18:3 cis-9, cis-12, cis-15; C18:2 cis-9, trans-11; C20:2 cis-11, cis-14; C20:3 n-6; C20:3 n-3; C20:4 n-6; C20:5 n-3; C22:6 n-3. 5 HP-PUFA: highly peroxidizable polyunsaturated fatty acids; calculated as the sum of PUFA with three or more unsaturated bonds. 6 SEM: standard error of the means. 7 NS: not significant (P > 0.05). 1

the former due to the lower dry matter intake, which could have impaired the accumulation of glycogen in muscle. Besides other factors, the development of meat colour after the oxygenation of the meat surface (blooming) is believed to be dependent on the final pH of the muscle, with meat lightness (L* values) being generally lower in meat with high ultimate pH (Confort & Egbert, 1985; Young, Priolo, Simmons, & West, 1999). This has been proposed as a possible explanation for the lower lightness (lower L* values) often observed in meat from pasture-fed animals compared to that from concentrate-fed ones (Priolo et al., 2001). In the present study, no differences in meat lightness were observed between meat from concentrate-fed animals (S) and meat from pasture-fed lambs (8 h and 4 h-PM treatments) and this could be partially attributed to the fact that the pH of LM from S-fed animals did not differ from those found in muscle from animals in both the 8 h and the 4 h-PM groups. However, in the present study, despite the fact that the restriction of the time at pasture (4 h-PM treatment) produced higher pH values in muscle compared to the 8 h treatment, no differences in lightness were observed among treatments (Table 1). These results, together with a lack of difference in meat redness (a*) and saturation (C*) between treatments, confirm previous findings showing that, in both cattle (French et al., 2000a) and lambs (Luciano et al., 2009), differences in meat colour between concentrate- and pasture-fed animals are not evident when animals are allowed to grow at comparable rates. Moreover, it is also evident that restricting the time at pasture did not impact negatively on meat colour compared to an 8-hour grazing duration. 3.3. Muscle oxidizable fatty acids, lipid oxidation and colour stability Intramuscular fat content and fatty acid composition are key factors to consider when the effect of diet on meat oxidative stability is investigated. In ruminants, ad libitum consumption of concentrate feeds has been often reported to produce fattier carcasses and higher intramuscular fat (IMF) content compared to pasture-based feeding systems because of the higher energy intake associated with concentrate rations (French et al., 2000b). Aurousseau, Bauchart, Calichon, Micol, and Priolo (2004) reported higher IMF contents in muscle from lambs fed concentrate in stall compared to animals grazing herbage at pasture with both groups allowed to grow at similar rates. Moreover, Vasta et al. (2009) found higher IMF contents in muscle from lambs fed concentrates compared to those given herbage with animals being individually penned indoors and allowed to grow at similar rates. Therefore, the

G. Luciano et al. / Meat Science 92 (2012) 30–35

higher IMF content found here in the LM from lambs fed concentrates (S) compared to animals raised on pasture either for 8 or for 4 h (P b 0.0005) were not surprising. Interestingly, it was found that the severe reduction in the time allowed at pasture for lambs in the 4 h-AM group and the consequent reduction in the dry matter intake did not compromise fat deposition in muscle, with IMF values similar to those measured in the LM from lambs allowed to graze for 8 h (Table 2). As previously stated, with respect to meat lipid oxidation, the concentration of PUFA in muscle is important as they represent preferential substrates for the oxidative reactions (Morrissey et al., 1998). However, the susceptibility of fatty acids to the oxidation increases as their unsaturation increases and, for example, the resistance to peroxidation of linoleic acid (LA, cis-9, cis-12 C18:2) is more than two-fold higher compared to that of linolenic acid (LNA, cis-9, cis-12, cis-15 C18:3; Shahidi, 1992). For this reason, although highly unsaturated fatty acids represent quantitatively minor components, small changes in their concentration can produce significant effects on meat oxidative stability (Yang et al., 2002). In the present study a higher proportion of PUFA in the IMF from lambs given concentrate feeds compared to those allowed to graze for 8 h was found (P b 0.0005; Table 2), although concentrate-based diets have often been reported to impair the deposition of PUFA in muscle compared to herbage-based diets (Wood & Enser, 1997). This result may be partially attributed to the much higher concentration of LA in the concentrate compared to the herbage (55.37 vs 13.55% of the total fatty acids, respectively (Data not shown). The ruminal biohydrogenation of dietary PUFA may proceed at a lower rate when animals receive concentrate-based diets due to the shorter rumen transit of concentrates compared to herbage, with a consequent limitation of the hydrogenation of PUFA (Doreau & Ferlay, 1994). This fact, together with the higher affinity of LA compared to LNA for incorporation into phospholipids (Wood et al., 2008) may explain the higher proportion of LA in the IMF from animals in the S group compared those in the 8 h group (16.58% vs 8.68%; P b 0.0005 (Data not shown)). Nevertheless, when the highly peroxidizable fatty acids (HP-PUFA) with more than two double bonds were considered, their proportion was higher in the IMF from animals raised at pasture (8 h and 4 h-PM groups) compared to lambs in the S treatment (P b 0.001; Table 2). This agrees with other findings showing a greater deposition of highly unsaturated PUFA consequent to pasture-based diets compared to concentrate-based ones (Descalzo et al., 2005; Yang et al., 2002). As reported by Vasta et al. (2012a), higher levels of PUFA were found, in the present study, in LM from lambs in the 4 h-PM treatment compared to those in the 8 h group (P b 0.0005; Table 2). Moreover, restricting the time at pasture (4 h-PM) also increased the concentration of HP-PUFA in the IMF compared to the 8 h treatments (P b 0.001). Vasta et al. (2012a) hypothesized that the diurnal variation in the fatty acid profile in herbage favoured the accumulation of LNA in the afternoon and this might have contributed to increase the concentration of PUFA in muscle from lambs in the 4 h-PM group. In the present study, as the diet affected meat fat content, expressing the classes of fatty acids as percentages of total fat may not be particularly relevant in discussing the susceptibility of muscle to lipid oxidation. Animals given concentrates (S group) had a higher IMF content and, therefore, a higher absolute content of the readily oxidizable fatty acids (PUFA and HP-PUFA) per unit of muscle compared to lambs allowed to graze at pasture (8 h and 4 h-PM groups). Fig. 1 clearly shows the strong effect of the dietary treatment (P b 0.0005) and the Time × Diet interaction (P b 0.0005) on lipid oxidation. Meat from animals in the 8 h and 4 h-PM groups had a high resistance to lipid oxidation, with TBARS values increasing significantly after 10 days of storage (P b 0.05) and being low throughout storage. Conversely meat from lambs in the S group was unstable and TBARS values increased significantly after only 3 days (P = 0.02) and, thereafter, up to 7 days (P = 0.03). Moreover, TBARS values measured in meat from lambs in the S group after only 3 days were higher than

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Fig. 1. Effect of treatment (8 h, 4 h-PM or S) and time of storage (days 0, 3, 7, and 10) on TBARS values (mg MDA/kg meat) of raw LM stored over 10 d at 4 °C. Values are means plus standard deviations. Treatments were: 8 h = lambs fed exclusively at pasture for 8 h (from 9 am to 5 pm); 4 h-PM = lambs fed exclusively at pasture for 4 h in the afternoon (from 1 pm to 5 pm); S = lambs fed exclusively concentrates in stall. a,b,c,d Values with different superscripts are significantly different (P ≤ 0.05).

those reached in meat from both the 8 h and the 4 h-PM groups after 10 days (P=0.001 and P=0.02, respectively). These results agree with a number of reports demonstrating that, compared to concentratebased diets, feeding systems based on green forages confer on meat a superior resistance to oxidative deterioration due to the high concentrations of antioxidants in green herbage which can effectively counteract the oxidation of fatty acids (Faustman et al., 2010; Wood & Enser, 1997). Interestingly, the restriction of time at pasture (4 h-PM treatment) did not produce any detrimental effect on meat lipid oxidation compared to the 8 h treatment. Compared to lambs in the 8 h group, animals in the 4 h-PM treatment had a higher concentration of PUFA and HP-PUFA in the IMF. This, together with a possible lower intake of antioxidants in the 4 h-PM animals consequent to the lower herbage intake, might have been expected to impair the oxidative stability of meat from this group. In pigs fed a concentrate-based diet, Mason et al. (2005) reported lower vitamin E concentration in muscle consequent to feeding restriction, while Savary-Auzeloux et al. (2008) showed that restriction of feed intake in concentrate-fed lambs consistently reduced muscle's antioxidant status. However, it should be noticed that, compared to concentrate-feeds, fresh herbage generally contains greater amounts of antioxidants (Wood & Enser, 1997). Moreover, in the case of vitamin E for example, green herbage contains much higher proportions of the readily bioavailable RRR-α-tocopherol stereoisomer compared to concentrates, which results in a higher deposition of vitamin E in muscle from animals fed herbage than in that from concentrate-fed ones even if both diets provide similar amounts of vitamin E stereoisomers (Röhrle et al., 2011). Furthermore, Yang et al. (2002) and Descalzo et al. (2005) found that supplementing vitamin E to herbage-based diets did not increase vitamin E levels in muscle and plasma of cattle and did not improve meat oxidative stability, which demonstrates that pasture-based diets can provide sufficient vitamin E to saturate its deposition in tissues and to delay meat oxidative deterioration. In the present study, although vitamin E and other antioxidants in muscle were not measured, it is likely that lambs in the 4 h-PM treatment accumulated sufficient antioxidants to protect meat against lipid oxidation, despite the lower herbage intake and the higher PUFA and HP-PUFA levels in muscle compared to animals not subjected to the restriction of grazing time. Research has provided evidence for a positive effect of pasturebased feeding systems in extending meat colour stability compared to intensive concentrate-based diets (Renerre, 2000). The deterioration of meat colour is mainly dependent on the oxidation of myoglobin which is promoted by the oxidation of fatty acids (Faustman et al., 2010). Therefore, the protective effect of feeding systems based on the consumption of fresh herbage against meat lipid oxidation can partially explain the improved colour stability generally observed in meat from pasture-fed animals. The decrease of meat redness (a* values) over time of storage or display is often used to describe meat discolouration

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to feeding systems based on concentrates. Additionally, as observed for lipid oxidation, the restriction of the grazing duration did not produce detrimental effects on meat colour stability. 4. Conclusions

Fig. 2. Effect of treatment (8 h, 4 h-PM or S) and time of storage (days 0, 3, 7, and 10) on (a) a* values and (b) H* values of raw LM stored aerobically over 10 d at 4 °C. Values are means plus standard deviations. Treatments were: 8 h = lambs fed exclusively at pasture for 8 h (from 9 am to 5 pm); 4 h-PM = lambs fed exclusively at pasture for 4 h in the afternoon (from 1 pm to 5 pm); S = lambs fed exclusively concentrates in stall. a,b,c,d,eValues with different superscripts are significantly different (P ≤ 0.05).

as it correlates well with the sensory evaluation of meat colour deterioration (Insausti, Beriain, Lizaso, Carr, & Purroy, 2008; Mancini & Hunt, 2005). In the present study, a general decrease in meat redness over storage was observed (P b 0.0005; Fig. 2a). Moreover, while the dietary treatment did not affect meat redness, a significant Time× Diet interaction (P = 0.04) indicated a different pattern of change in a* values over time related to dietary treatment. Indeed, differences in meat redness between treatments were never detected during storage; however, from 3 to 10 days while a* values decreased in meat from lambs in both the S and 8 h treatments (P = 0.001), they remained stable in meat from the 4 h-PM animals. This suggests that the restriction of time at pasture improved the stability of the red colour typical of fresh meat. However, redness measurements did not show differences in meat colour stability between pasture- and concentrate-fed animals. Other descriptors have been used for evaluating meat colour stability. The increase in hue angle (H* values) over time, for example, correlates well with metmyoglobin accumulation at the meat surface and, therefore, can give a reliable perspective of meat browning (Luciano et al., 2011). A general increase in H* values during storage, regardless of the dietary treatment was found (P b 0.0005; Fig. 2b). However, the dietary treatment affected this colour parameter (P = 0.03) and a significant Time × Diet interaction (P b 0.0005) indicated a different rate of increase in H* values depending on dietary treatment. Indeed, while from 3 to 10 days H* values did not change in meat from lambs raised at pasture (8 h and 4 h-PM treatments), they increased in meat from animals in the S group (P b 0.0005). Furthermore, this different rate of change in hue angle values among treatments accounted for the higher H* values (higher meat browning) measured after 10 days in meat from animals fed concentrates (S) compared to that from lambs raised at pasture (8 h and 4 h-PM groups; P b 0.05). These results confirm the protective effect of herbage-based diet against meat discolouration compared

The results of the study confirms that feeding lambs fresh herbage at pasture results in a general improvement of meat oxidative stability compared to a concentrate-based feeding system in stall. Specifically, the extent of lipid oxidation during storage showed the high oxidative instability of meat from concentrate-fed lambs compared to meat produced by feeding lambs at pasture. This could partially explain the higher colour stability observed in meat from pasture-fed lambs compared to that from concentrate-fed ones. Moreover, in the light of the results found, it is worth noting that a significant restriction of grazing duration from 8 to 4 h per day did not noticeably impair lamb growth performance and carcass yield. A possible adaptation of the grazing behaviour consequent to the restriction of the time at pasture could have allowed lambs to partially overcome such feeding restriction and to minimize detrimental effects. Additionally, the restriction of the grazing duration did not compromise any of the meat quality parameters studied, including muscle fat content, colour and oxidative stability. Conversely, feeding lambs at pasture for 4 h in the afternoon appeared to improve meat fatty acid composition with increase PUFA in the intramuscular fat. In low-input farming systems, reducing the exploitation of pastures and the burden linked to the care of animals at pasture may be of interest. The results of the present study motivate further research aiming at better understanding the adaptation of ruminants to a reduction of grazing duration. Also, the study of the effects of the pasture quality and botanical composition on lamb performances and meat quality in response to a restriction of the grazing duration should be focused on. Acknowledgments The authors gratefully acknowledge funding from the European Community financial participation under the Seventh Framework Programme for Research, Technological Development and Demonstration Activities, for the Integrated Project LOWINPUTBREEDS FP7CP-IP 222623. The views expressed in this publication are the sole responsibility of the authors and do not necessarily reflect the views of the European Commission. Neither the European Commission nor any person acting on behalf of the Commission is responsible for the use which might be made of the information contained herein. References Aurousseau, B., Bauchart, D., Calichon, E., Micol, D., & Priolo, A. (2004). Effect of grass or concentrate feeding systems and rate of growth on triglyceride and phospholipid and their fatty acids in the M. longissimus thoracis of lambs. Meat Science, 66, 531–541. Avondo, M., Bordonaro, S., Marletta, D., Guastella, A. M., & D'Urso, G. (2002). A simple model to predict the herbage intake of grazing dairy ewes in semi-extensive Mediterranean systems. Livestock Production Science, 73, 275–283. Confort, D. P., & Egbert, W. R. (1985). Effect of Rotenone and pH on the color of prerigor muscle. Journal of Food Science, 50, 34–44. Descalzo, A. M., Insani, E. M., Biolatto, A., Sancho, A. M., García, P. T., Pensel, N. A., et al. (2005). Influence of pasture or grain-based diets supplemented with vitamin E on antioxidant/oxidative balance of Argentine beef. Meat Science, 70, 35–44. Descalzo, A. M., & Sancho, A. M. (2008). A review of natural antioxidants and their effects on oxidative status, odor and quality of fresh beef produced in Argentina. Meat Science, 79, 423–436. Doreau, M., & Ferlay, A. (1994). Digestion and utilisation of fatty acids by ruminants. Animal Feed Science and Technology, 45, 379–396. Faustman, C., Sun, Q., Mancini, R., & Suman, S. P. (2010). Myoglobin and lipid oxidation interactions: Mechanistic bases and control. Meat Science, 86, 86–94. Folch, J., Lees, M., & Stanley, S. G. H. (1957). A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry, 226, 497–509.

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