Effects of age and season of slaughter on meat production of light lambs: Carcass characteristics and meat quality of Leccese breed

Small Ruminant Research 114 (2013) 97–104

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Effects of age and season of slaughter on meat production of light lambs: Carcass characteristics and meat quality of Leccese breed Angela Gabriella D’Alessandro a,∗ , Giuseppe Maiorano b , Marco Ragni a , Donato Casamassima b , Giuseppe Marsico a , G. Martemucci a a b

Dipartimento di Scienze Agro-Ambientali e Territoriali, Università degli Studi di Bari, Via G. Amendola, 165/A, 70126 Bari, Italy Dipartimento Agricoltura, Ambiente e Alimenti, Università degli Studi del Molise, Via F. De Sanctis snc , 86100 Campobasso, Italy

a r t i c l e

i n f o

Article history: Received 9 January 2013 Received in revised form 22 April 2013 Accepted 9 May 2013 Available online 24 June 2013 Keywords: Light lamb Age Slaughter season Carcass traits Meat quality

a b s t r a c t The effects of the slaughter season (winter and spring) and the age at slaughter (45 and 60 days) on the carcass characteristics and physico-chemical quality of meat were investigated on 40 Leccese lambs. In each season, 20 lambs were subdivided into two groups corresponding to the experimental ages. All lambs received maternal milk and a supplementation of hay and commercial concentrate from 30 days to slaughter. The ewes were fed a basal mixed diet (unifeed) and commercial concentrate and were allowed to graze for 5 h a day on polyphytic cultivated grassland. The increase of the lambs’ slaughter age from 45 to 60 days resulted in an improvement in live weight, some commercial cuts (shoulder and loin), the majority of the carcass measurements, adiposity and conformation of shoulder and leg and the muscle/fat ratio. Intramuscular collagen properties were also affected by slaughter age. Considering the slaughter seasons, the best results have been obtained in spring and have been maximised in lambs slaughtered at 60 days that showed the greatest live weight (16 kg), good percentages of commercial cuts and carcass measurements, the greater levels of adiposity and better conformations of shoulder and leg and the lowest Warner–Bratzler (WB) shear force, without substantial difference in relation to colorimetric indices of meat. In conclusion, age and season of slaughter should be considered for the traditional production of light lambs. Lambs slaughtered in spring at 60 days of age showed the better characteristics of the carcasses and quality of meat. © 2013 Elsevier B.V. All rights reserved.

In recent years, with increasing emphasis on sustainable farming systems, the use and exploitation of local breeds have elicited particular attention. These breeds are known to be less productive than allochthonous and/or more selected breeds, but the growing demand for animal products due to economic, political and social pressures has led to the consideration of local breeds that are not suitable

∗ Corresponding author. Tel.: +39 0805442524; fax: +39 0805442828. E-mail address: [email protected] (A.G. D’Alessandro). 0921-4488/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.smallrumres.2013.05.006

for current needs or those of the immediately perceived future (Barker, 1999). Leccese sheep is an endangered Italian local breed that was once widespread in the Apulia region but suffered a drastic contraction in population size during the past three decades (Siculella et al., 2008; Cecchi et al., 2008). The current count of this breed is approximately 2000 animals (Castellana et al., 2008). The strengths of this breed are its adaptability also in marginal areas, high resistance to local parasites and high quality of both lamb meat and milk production (Castellana et al., 2008; D’Alessandro et al., 2012). These characteristics of the Leccese breed

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imply its potential use in an eco-sustainable or organic breeding system based on pasture and the obtaining of products having peculiar characteristics closely linked to the territory. Recently, meat from the Leccese breed has been considered within the collective quality brand with the indication of origin ‘Prodotti di Qualità Puglia’, submitted to the European Union for the recognition. For the ewes, semi-extensive or semi-stabled systems using pasturage are the most frequent practises. Lambs are traditionally reared under a milking–suckling system and are fed exclusively with maternal milk or with a moderate supplementation of feeding at the end of the breeding period. Lambs stay with their mothers all night after the afternoon milking and are separated from them in the morning. The traditional consumption peaks of lamb meat are Easter and Christmas, with slaughters occurring in the winter (December–January) and in the spring (March–April). The lamb production system follows closely that which is widely used for dairy breeds in Mediterranean countries. However, in lamb meat production systems, higher productivity and more flexibility may be gained by a small increase in the lamb’s weight (Santos-Silva et al., 2002). There is very little information available on meat production from light lambs of autochthonous breeds reared in southern Italy. Therefore, the aim of this study was to determine whether the age and season at slaughter affect the carcass traits and meat quality (as defined by physical and chemical characteristics) of Leccese light lambs reared under common management and in the traditional periods.

to the Animals (Scientific Procedures) Act (ASPA) (1991) procedures. Hot and cold carcass weights were recorded, and the dressing percentages were calculated after dressing and chilling at 2–4 ◦ C for 24 h. The carcass shrink losses, calculated as the difference between the hot and cold carcass weights, were expressed as a percentage of the hot carcass weight. Linear carcass measurements were taken on the cold carcasses 24 h post mortem. The shoulder, loin and leg were scored for the adiposity rate on a scale of 1–5 (1 = very lean, 5 = very fat). Moreover, the shoulder and leg conformation were rated on a ranking from 1 (poor) to 5 (excellent). The left side of the carcass was dissected into commercial cuts (neck, cutlet and breast, shoulder, loin, bacon and leg), kidney and perirenal fat. The hind leg, loin and shoulder were then dissected into their main tissue components (lean, subcutaneous and intermuscular fat and bone) (ASPA, 1996). The lean/bone and lean/fat ratios were determined. 1.3. Meat analyses 1.3.1. Physical characteristics The pH of the longissimus dorsi (LD) muscle was measured 45 min and 24 h (ultimate pH) after slaughter using a portable pH meter (Eutech Instruments, mod. XS pH 600, Singapore) equipped with a penetrating glass electrode. The colorimetric indices (lightness, L*; redness, a*; yellowness, b*) on the LD muscle were determined using a HunterLab MiniScanTM XE spectrophotometer (mod. 4500/L, 45/0 LAV, 3.20 cm diameter aperture, 10◦ standard observer, focussing at 25 mm, illuminant D65/10; Hunter Associated Laboratory, Inc.; Reston, VA, USA), taking three readings for each sample. The reflectance measurements were performed after the samples had oxygenated in air for at least 30 min, by which time the measurements ˇ ˇ and Candek-Potokar, 2006). were stable (Skrlep 1.3.2. Chemical composition The chemical composition was analysed on homogenised raw meat samples (250 g) from the longissimus lumborum (LL) muscle. Moisture, protein, lipid and ash content in each sample were determined according to the ASPA procedures (1996).

1. Materials and methods The animal handling followed the recommendations of European Union directive 86/609/EEC and Italian law 116/92 regarding animal care. 1.1. Experimental design, location and animal management The study was conducted on a farm located in southern Italy (latitude: 40◦ 49 48 72 N, longitude: 16◦ 33 16 20 E) at 500 m above sea level. The climate of this area is sub-coastal, with approximately 600 mm of annual rainfall and moderately cold winters (an average temperature of 5.5 ◦ C) and hot, dry summers (an average temperature of 22 ◦ C). The trial was carried out on 40 Leccese male lambs in the winter and spring, during the traditional consumption peaks, Easter and Christmas. In the autumn and spring, 20 lambs born as singles from dams homogeneous for age (3.5 years), weight (51 ± 2.0 kg) and milk yield were considered. At birth, the lambs were divided into two groups of 10 animals each, homogeneous for weight (4.10 ± 0.2 kg) and corresponding to the experimental slaughter ages, according to a factorial scheme of 2 × 2 (two seasons – winter and spring and two slaughter ages – 45 and 60 days). Each group was then subdivided into two subgroups of five animals each. The lambs stayed with their respective mothers between 18:00 and 08:00 of the following day and received maternal milk and a supplementation of hay and commercial concentrate (barley, corn and faba beans; 20% protein, 2.5% fat, 4% cellulose and 6.9% ash) from 30 days to slaughter. Throughout the trial, the ewes were fed a basal mixed diet (unifeed; 1400 g head−1 day−1 ) that consisted of chopped oat hay, clover, vetch and rye grass (800 g), commercial feed (200 g) and water (400 g). In addition, the ewes were allowed to graze for 5 h a day on polyphytic cultivated grassland (40% barley, 40% oats, 10% wheat, 2% rye grass and 8% clover) and received a commercial concentrate (barley, corn and faba beans; 15% protein, 2.5% fat, 6% cellulose and 6.7% ash; 140 g head−1 day−1 ) during milking. 1.2. Animal slaughtering and assessment of carcass characteristics In each season, one group of lambs was slaughtered at 45 days of age and the other group was slaughtered at 60 days. The animals were slaughtered after 12 h fasting at a local slaughterhouse and processed according

1.3.3. Collagen analyses The intramuscular collagen (IMC) analyses were performed on the semimembranosus muscle (SM). Samples of SM were removed from the left leg of each carcass (after 24 h at 2–4 ◦ C), vacuum packaged and stored in a freezer (−40 ◦ C) until analysis. For the IMC analyses, the SM samples were thawed overnight at 4 ◦ C, trimmed of fat and epimysium, lyophilised for 48 h, weighed and hydrolysed in Duran tubes in 6 N HCl at 110 ◦ C for 18–20 h (Etherington and Sims, 1981) to determine the hydroxyproline (Woessner, 1961) and crosslinking. All of the analyses were performed in duplicate. The IMC concentration was expressed as ␮g hydroxyproline/mg of lyophilised tissue. The hydroxylysylpyridinoline (HLP) concentration, the principal non-reducible crosslink of muscle collagen (McCormick, 1999), was determined as described by Maiorano et al. (2012) and expressed as both moles of HLP per mole of collagen and ␮g HLP/mg of lyophilised tissue (Maiorano et al., 2007). 1.4. Statistical analyses The data were analysed using the GLM procedure of SAS (2002). For the data on the slaughter performance, the carcass characteristics and the chemical composition of the meat, the model considered the effects of the season (two levels: winter and spring, with the error term being individual within a given season), the lambs’ slaughter ages (two levels: 45 and 60 day of age, with the residual error being the error term), their interaction and the random effects of individual and residual. The means were compared using the t-test and the significance was declared at P < 0.05.

2. Results and discussion 2.1. Slaughter performance The final live weight achieved by the lambs was affected by the slaughter season (P < 0.01) and, as expected, by the slaughter age (P < 0.05; Table 1). The live weight of the lambs at 45 days of age is consistent with that reported

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Table 1 Effects of age (SA) and season (SS) of slaughter on performance and carcass commercial cuts. Winter

Spring

Root MSE

Effectd

45 d

60 d

45 d

60 d

(df = 36)

SA

SS

SA × SS

N. of lamb Fasting live weight (kg)

10 12.08

10 13.29A

10 12.79A

10 16.40B

1.79

*

**

NS

Empty body weighte (kg) Hot carcass weight (kg) Cold carcass weight (kg) Hot dressing (%) Cold dressing (%)

10.60 7.41 7.27 69.71 68.43

11.73A 8.29A 8.06A 70.09 68.9

11.35A 8.20A 7.92A 67.45 65.15

15.10B 10.79B 10.53B 69.24 67.56

1.59 1.15 1.12 3.87 3.63

** ** ** NS NS

** ** ** NS NS

NS NS NS NS NS

Carcass cuts (%) Neck Cutlet and breast Shoulder Loin Bacon Leg Kidney Perirenal fat

8.24a 23.70A 21.15A 8.03A 3.20 33.23 0.98A 0.98a

9.99Ab 18.83B 23.50B 10.35B 3.26 32.11 1.28B 0.67b

8.89 22.77 19.00B 9.28 2.83 34.93A 1.16A 1.20A

7.92B 23.84A 21.37A 9.60 2.95 32.49B 0.97B 0.84B

1.21 1.89 1.58 1.46 0.60 1.66 0.25 0.29

NS ** ** ** NS ** NS **

** ** ** NS NS * NS *

** ** NS * NS NS ** NS

c

A,B,C

P < 0.01. P < 0.05. c MSE = mean square error. d Significance level: NS = non-significant, P > 0.05; *P < 0.05; **P < 0.01. e Body weight excluding contents of the gastro-intestinal tract.

a,b

in other studies on Leccese lambs (Vicenti et al., 2002). At 60 days of age, the lambs showed the greatest final weight when slaughtered in the spring (P < 0.01). Considering that the feeding management of the lambs and their mothers was consistent in the two rearing periods, the higher live weight of lambs in the spring could be attributed to the maternal milk composition, which may be positively affected by the greater availability and/or better quality of pasture in this season. It has been reported that variations of milk composition depended on the grazed plant species, their vegetative stage and the diets of the ewes (Addis et al., 2005; Morand-Fehr et al., 2007). Overall, the carcasses obtained in this study had a weight which can be classified as class B and C in the European carcass classification system for light lambs (≤7, 7.1–10 and 10.1–13 kg; EU, 1994). The carcass weight of the lambs was affected by the slaughter age only in the spring (P < 0.01), with a greater value at 60 days of age. Considering the effect of the season, the carcass weights of the lambs was heavier in the spring in comparison with the winter (P < 0.01). By contrast, Mazzone et al. (2010) found that the carcass weight of Apennine suckling lambs tended to be lower during the slaughter at Easter. Despite the differences found in the carcass weights, the dressing percentages were not affected (P > 0.05) by the slaughter season or the slaughter age of the lambs (Table 1). In another study on Greek mountain breed lambs (Skapetas et al., 2006), the highest dressing percentage was observed at the slaughter age of 45 days, with a decrease at 60 days and a further increase at 75 and 90 days of age. These findings were attributed to the highest growth rate of lambs at 45 days of age, which decreases at 60 day due to the weaning stress that usually decreases the weight gains. To our knowledge, no information is available from current literature on growing rate and slaughter performance of Leccese lambs at >60 days of age.

The slaughter age markedly influenced the carcass proportion of the commercial cuts of lambs slaughtered in the winter; in fact, compared to lambs of 45 days of age, those of 60 days had higher percentages of neck (P < 0.05), shoulder (P < 0.01) and loin (P < 0.01) and lower (P < 0.01) percentages of cutlet and breast (Table 1). In the spring, the differences due to the slaughter age were observed for the proportions of shoulder and leg, which were greater (P < 0.01) in 60-day and 45-day lambs, respectively. In addition, the perirenal fat percentage was affected by both the age (P < 0.01) and the season (P < 0.05); it was higher in lambs slaughtered at 45 days compared to animals of 60 days, and, in general, was higher in lambs slaughtered in the spring. An interaction (P < 0.01) between the age and season was observed for the kidney percentage. The changes in the commercial cuts of the carcass with the slaughter weight have been attributed to the different growth of tissues of the body regions relative to the whole body (Butterfield et al., 1984; Teixeira et al., 1996). The results of our study led us to hypothesise that in lambs slaughtered in the spring, a more constant and isometric growth rate occurred until 60 days of age, which could have been promoted by the environmental conditions and/or maternal milk availability. By contrast, the results obtained in the winter seem to show a marked increase in the growth rate of the lambs from 45 to 60 days. The commercial cuts’ proportions obtained by the Leccese lambs (slaughter weight 12–16 kg) were similar to ˜ lambs (slaughter weight those reported for the Segurena 19–25 kg), a major Spanish meat breed that obtained the Protected Geographic Indication (PGI) in 2008, except for the greater proportion of loin observed in our study (from ˜ lambs; Pena ˜ et al., 8.0% to 10.3% vs. 7% for the Segurena 2005). This parameter, which is connected to the body conformation of the animals, was influenced by the greater slaughter weights at 60 days, in agreement with a study on

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Table 2 Effects of age (SA) and season (SS) of slaughter on carcass characteristics. Winter

Spring

Root MSE

Effectd

45 d

60 d

45 d

60 d

(df = 36)

SA

SS

SA × SS

44.44a 12.45 11.85A 46.45 12.68 20.32A

47.15Ab 12.78A 14.10B 48.55 13.35A 28.75BC

46.10A 12.70A 11.37A 46.30A 12.45A 26.47B

51.40B 14.20B 12.90B 50.40B 14.85B 29.05C

2.52 1.19 0.70 2.32 0.95 3.27

* * ** * ** **

** * ** NS * **

NS NS NS NS NS NS

Shoulder adipositye Loin adipositye Leg adipositye

1.00A 1.50A 1.37A

2.00B 2.90B 2.00Ba

1.90B 2.55Ba 2.10B

2.20 2.30b 2.55b

0.55 0.61 0.51

** NS **

** ** **

NS ** NS

Shoulder conformationf Leg conformationf

1.75 2.25Aa

2.29 3.29B

2.00a 2.95b

2.60b 3.50

0.67 0.63

** **

NS *

NS NS

Left side length (cm) Thorax length (cm) Thorax depth (cm) Trunk length (cm) Back length (cm) Leg length (cm)

c

A,B,C

P < 0.01. P < 0.05. c MSE = mean square error. d Significance level: NS = non-significant, P > 0.05; *P < 0.05; **P < 0.01. e Rated on a scale 1–5 (1 = very lean, 5 = very fat). f Rated on a scale 1–5 (1 = poor, 5 = excellent).

a,b

Manchega suckling lambs (Díaz et al., 2006). By contrast, in English meat-type lambs, the age or the slaughter weight had no influence on the percentage of the first-grade cuts (leg long, last eight ribs-loin) (Kemster et al., 1987a). 2.2. Carcass characteristics The results of the carcass linear measurements and the conformation of some regions are presented in Table 2. The age and the slaughter season influenced (0.05 > P < 0.01) the majority of the measurements of the lamb carcasses. As expected, all of the parameters increased with the increase of the slaughter age, but in the spring, a more homogeneous growth rate was exhibited by lambs of 60 days (8.8% of trunk length to +19.3% of back length) in comparison with lambs slaughtered in the winter (+2.6% of thorax length to +41.5% of leg length). It is known that 70–80% of the peak bone mass is genetically determined and the remaining 20–30% is ascribed to environmental factors, of which nutrition is one of the most important (Eastell and Lambert, 2002). In line with the carcass measurements, the level of adiposity scored at the shoulder, loin and leg, as well as the shoulder and leg conformations, showed a significant and positive effect with the greater slaughter age (P < 0.01) and the spring season (0.01 > P < 0.05). All of the parameters were improved in lambs slaughtered in the spring at 60 days, except for the loin adiposity that, in this season, was greater (P < 0.05) in lambs slaughtered at 45 days. The hind leg is considered to be a good indicator of the overall carcass tissue composition, especially the fatness ˜ (Guía and Caneque, 1992). In the present study, we considered the dissection of the shoulder, loin and leg as indices of the tissue composition of the lamb carcass. Table 3 shows the proportion of the lean, fat and bone tissues obtained by the dissection of the shoulder, loin and leg and the main indices of lean/bone and lean/fat ratios. The slaughter age affected (P < 0.01) the shoulder weight and its lean and fat percentages, the loin weight and its lean percentage

and the leg weight (P < 0.01) and the lean (P < 0.01) and fat (P < 0.05) percentages of the leg. The effect of the slaughter season was significant for the percentages of the shoulder bone (P < 0.01) and fat (P < 0.05) and for the leg weight and its bone and fat percentages (P < 0.01). The interaction between the main fixed effects (slaughter age × season) was significant for all of the shoulder parameters (weight and lean, fat and bone content; 0.01 > P < 0.05), the lean percentage in the loin (P < 0.01) and leg weight (P < 0.01). The lean/bone ratio was affected by the season (P < 0.01) with the most favourable index occurring in the spring (0.05 > P < 0.01). No differences were found between the slaughter ages of the lambs. The lean/fat ratio depended on both the slaughter age (P < 0.01) and the season (P < 0.05), and the greatest (0.05 > P < 0.01) value was obtained in the winter in 60-day lambs. It is known that in livestock animals, bone growth occurs earlier with respect to lean and fat (Kemster et al., 1987b; Taylor et al., 1989), and this has been attributed to a change in the priority of use of the nutrients by the body tissues during the life of the animals. In the present study, the age at slaughter influenced only the lean/fat ratio. Overall, from a physiological point of view, these results may reflect differences in the growth patterns of the lamb carcass regions and allow us to assume that in our production system, the body tissues’ development may have been affected by the environmental conditions related to the season, leading to a differential growing rate of the lambs. Accordingly, the best conditions have corresponded to the lamb slaughter in the spring.

2.3. Physical characteristics of meat The physical characteristics of lamb meat are shown in Table 4. The ultimate pH was affected (P < 0.01) by the season, showing greater values in the winter compared to the spring, while the pH values were similar between the slaughter ages studied. It is known that the lower values of pH may be due to greater contents of muscle glycogen (Beriain et al., 2000), and this, in turn, could be influenced

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Table 3 Effects of age (SA) and season (SS) of slaughter on lean, fat and bone content in shoulder, loin and leg. Winter

Spring

Root MSE

Effectd

(df = 36)

SA

SS

SA × SS

Shoulder weight (g) Lean (%) Fat (%) Bone (%)

749.10Aa 52.52A 13.22A 44.25Aa

650.28Ab 54.17Ba 6.05B 39.78b

828.87B 50.82B 12.60 36.58B

883.05C 49.24b 12.30A 38.46

95.97 4.97 3.97 4.50

** ** ** NS

NS NS * **

** ** ** *

Loin weight (g) Lean (%) Fat (%) Bone (%)

236.45 46.40A 10.48 43.12

286.99 34.40B 17.37 48.23

225.76A 42.22 15.31 42.47

333.71B 41.71A 15.24 43.05

61.46 5.22 6.36 6.69

** ** NS NS

NS NS NS NS

NS ** NS NS

1170.00 55.11 7.14 37.75a

1010.50A 57.53 5.17 37.29b

1070.20A 54.84A 12.27a 32.88

1387.20B 60.01B 7.96b 32.03a

160.96 3.81 3.93 4.83

NS ** * NS

** NS ** **

** NS NS NS

1.53B 4.70

1.53b 5.62b

0.25 2.30

NS **

** *

NS NS

45 d

Leg weight (g) Lean (%) Fat (%) Bone (%) Lean/bone ratioe Lean/fat ratioe

60 d

1.23A 5.28A

45 d

1.33a 8.16Ba

60 d

c

A,B,C

P < 0.01. P < 0.05. c MSE = mean square error. d Significance level: NS = non-significant, P > 0.05; *P < 0.05; **P < 0.01. e Calculated considering the total weight of shoulder, loin and leg.

a,b

by the lamb-feeding regimen. We believe that, in our study, the lower values of pH in the spring could be attributed to the characteristics of the milk that the lambs took from their mothers. In fact, the quantity of milk, as well as the lactose and fat content, have been positively linked to the production of muscle glycogen (Beriain et al., 2000). Accordingly, the age of the lambs did not have any effect, although the lambs at 60 days had taken a greater amount of concentrate compared to the lambs slaughtered at day 45, and the concentrate promotes ruminal fermentation and thus the production of propionic acid, which is the precursor of muscle glycogen (Vernon, 1981). Our results agree in part with those of a study on Appenninica lamb meat, where higher pH values were observed in the winter compared to the autumn (Mazzone et al., 2010). The pH values observed in this study, accepted for commercial meats, were similar to the results from other studies (Juárez et al., 2009; Maiorano et al., 2009) and were lower compared to our previous study on Leccese lambs (D’Alessandro et al., 2012). In the latter, the lighter slaughter weight of lambs might have determined a high ultimate pH because an undernourished

condition has been associated with a reduction of the glycogen reserves in muscles (Bray et al., 1989). The carcass shrink losses were not affected (P > 0.05) by the slaughter age of the lambs or by the season (Table 4). The colour of the meat is an extremely important parameter for consumer judgement of the freshness and quality of meat (Martinez-Cerezo et al., 2005; Mancini and Hunt, 2005), and a pale or pink colour is required for light lamb meat. In the present study, the lightness values (L*) for all of the groups, ranging between 46.3 and 49.8, are indicative of pale meat. No differences were observed between the different ages within each season. However, for the 60-day lambs, a darker (P < 0.05) colour was found in the meat of lambs slaughtered in the winter compared to that of the animals slaughtered in the spring. No differences (P > 0.05) were found in the redness (a*) or in the yellowness (b*). The greater value of the L* index in lambs of 60-day lambs slaughtered in the spring could be attributable to the heavier body weights of the lambs obtained in the spring compared to those in the winter. By contrast, some authors (Teixeira et al., 2005; Wojtysiak

Table 4 Effects of age (SA) and season (SS) of slaughter on pH, shrink losses and colour. Winter 45 d pH at slaughter Ultimate pH Carcass shrink losses (%) Colour coordinates L* (lightness) a* (redness) b* (yellowness) A,B

6.61 5.96A 2.35 46.64 8.39 12.70

Spring 60 d 6.48 5.97A 1.84 46.30a 8.82 12.52

45 d 6.58 5.82B 3.32 48.80 8.08 12.67

P < 0.01. P < 0.05. c MSE = mean square error. d Significance level: NS = non-significant, P > 0.05; *P < 0.05; **P < 0.01.

a,b

Root MSE

Effectd

(df = 36)

SA

SS

SA × SS

6.58 5.77B 2.42

1.20 0.08 1.57

NS NS NS

NS ** NS

NS NS NS

49.77b 8.19 12.40

3.04 0.88 1.19

NS NS NS

NS NS NS

NS NS NS

60 d

c

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Table 5 Effects of age (SA) and season (SS) of slaughter on chemical composition (%) of longissimus lumborum muscle. Winter

N. Moisture Protein Total fat Ash

Spring

Effectd

Root MSE

45 d

60 d

45 d

60 d

(df = 36)

SA

SS

SA × SS

10 75.18 18.95 3.31 1.14Aa

10 75.43 19.16 3.27 1.27B

10 75.58 19.43 2.78 1.21b

10 75.45 19.94 3.08 1.11Aa

1.12 0.91 1.17 0.09

NS NS NS NS

NS NS NS NS

NS NS NS **

c

A,B

P < 0.01. P < 0.05. c MSE = mean square error. d Significance level: NS = non-significant, P > 0.05; *P < 0.05; **P < 0.01.

a,b

et al., 2010) reported that the lightness and the yellowness decreased with increasing live weight, whereas other studies (Russo et al., 2003; Maiorano et al., 2009) did not find any effect of live weight or carcass weight on the colour variables. Overall, the mean chromameter values (L*, a* and b*) for LD obtained in the current study were lower compared to our previous report on the meat of Leccese suckling lambs (D’Alessandro et al., 2012). The differences could be attributed to the effect of different feeding systems adopted in the two studies for both lambs and their mothers and the different ultimate pH values. 2.4. Chemical composition and collagen properties There were no significant (P > 0.05) differences for moisture, crude protein, fat and ash of LL in relation to the slaughter seasons and ages of lambs (Table 5). Significant interaction between the slaughter season and age (P < 0.01) was observed for the ash content. The results were comparable to those reported in other studies on suckling or light lambs of the Leccese (Vicenti et al., 2002; D’Alessandro et al., 2012) and Spanish (Juárez et al., 2009) breeds. Overall, the fat content values found in the present study could indicate a good quality of meat, in agreement with Wood (1990), who reported that a 2–3% intramuscular fat content is needed to ensure the good organoleptic qualities of meat. Meat is a complex, composite substance. It consists of myofibres, connective tissue and lipids. It has been established that collagen, the major component of the intramuscular connective tissue, plays a key role in

determining the background toughness of meat from different domestic animals (reviewed in Maiorano et al., 2012). The IMC properties in SM muscle are shown in Table 6. The IMC characteristics were not affected by the slaughter season. By contrast, with increasing slaughter age, a significant (P < 0.01) decrease in the IMC amount (−23%), and a significant (P < 0.01) increase in the collagen stability (+46%; mol of HLP/mol of collagen) and HLP concentration (␮g HLP/mg lyophilised tissue; P < 0.05) were found. There is remarkably little variation in the collagen concentration of the skeletal muscle with growth and age. Some exceptions are the elevated collagen concentrations in the muscle of very young animals compared to older animals (McCormick, 1994; Velleman et al., 1996). It is well established that with age, crosslinks progress from immature to more mature forms (e.g., HLP) (McCormick, 2009). These changes are related to the chemical nature of the covalent intermolecular crosslinks of collagen (reviewed in Nishimura, 2010). Some researchers reported that the shear force of raw meat is highly correlated with the collagen content. However, the correlation between the collagen content and the cooked meat toughness is usually lower (reviewed in Lepetit, 2008), and the crosslinks of collagen give rise to the toughness of the meat (Coro et al., 2003). On the other hand, McCormick (1999) reported that the role of collagen on the meat tenderness depends not only on the mature crosslinks but also on the amount of collagen. Maiorano et al. (2001) provide a tenderness index, which is the amount of HLP crosslinks per gram of lyophilised muscular tissue in different muscles in goat meat. In agreement with the suggestions of McCormick (1999) and Maiorano et al. (2001), the results of the HLP

Table 6 Effects of age (SA) and season (SS) of slaughter on collagen properties of semimembranosus muscle. Winter

IMCe (␮g/mgf ) HLPg (␮g/mgf ) HLP/IMC (mol/mol) A,B

Spring

Effectd

45 d

60 d

45 d

60 d

(df = 36)

SA

SS

SA × SS

39.20B 7.98a 0.142A

30.75A 8.98b 0.204B

38.80B 7.63a 0.137A

29.37A 8.46b 0.202B

0.59 0.11 0.003

** * **

NS NS NS

NS NS NS

P < 0.01. P < 0.05. c MSE = mean square error. d Significance level: NS = non-significant, P > 0.05; *P < 0.05; **P < 0.01. e Intramuscular collagen. f Of lyophilised muscular tissue. g Hydroxylysyl pyridinoline.

a,b

Root MSE c

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crosslink concentration (␮g/mg) indicate that the meat produced from younger lambs could be more tender than that from older animals. 3. Conclusions The variations among the meat characteristics in lambs slaughtered at different ages and seasons were observed. The increase of the lamb slaughter age from 45 to 60 days resulted in an improvement in the commercial cuts of the shoulder and loin, the majority of the carcass measurements, the adiposity and conformation of shoulder and leg and the lean/fat ratio as an index of the carcass tissues’ proportion. Furthermore, the increase in the chronological age increased the collagen maturity and the HLP concentration in the SM muscle lambs, which could affect the meat tenderness. Although the breeding system of lambs in the two seasons (winter and spring) has been fairly standardised, the slaughter season markedly influenced several parameters. Overall, the best results were obtained from the lambs slaughtered in the spring and were maximised with a slaughter age of 60 days. In particular, the lambs slaughtered in the spring at 60 days showed the greatest live weight, good percentages of commercial cuts and development of carcass measurements, greater levels of adiposity and better conformations of the shoulder and leg, without substantial differences in the colorimetric indices of the meat. The age and the slaughter season were not associated with the differences in carcass dressing percentages, the physical and chemical composition and the colorimetric indices. This study indicated that the breeding system for the production of the traditional light lamb meat has to consider the effects that the slaughter age and slaughter season have on the carcass characteristics and meat quality and support the recommendation of using 60 days as the slaughter age of the lambs of the Leccese breed. Acknowledgements This study was financially supported by Interreg III/A Greece-Italy (Project Code I 2101030, Paper N. 35) and by the University of Bari. The authors wish to thank Dr. Anna Morelli and Dr. Simona Tarricone for their support during the experimental work and Dr. Siria Tavaniello for chemical analyses of collagen; and Mr. Di Santo’s farm is greatly acknowledged for assistance in animal management. References Addis, M., Cabiddu, A., Pinna, G., Decandia, M., Piredda, G., Pirisi, A., Molle, G., 2005. Milk and cheese fatty acid composition of sheep fed different Mediterranean forages with particular reference to conjugated linoleic acid cis-9, trans-11. J. Dairy Sci. 88, 3443–3454. ASPA, 1991. Commissione metodologie di valutazione della produzione quanti-qualitativa della carne. Metodiche relative alla macellazione degli animali di interesse zootecnico e alla valutazione e dissezione della loro carcassa. ISMEA, Roma, Italy. ASPA, 1996. Metodiche per la determinazione delle caratteristiche qualitative della carne. Università di Perugia, Perugia, Italy. Barker, J.S.F., 1999. Conservation of livestock breed diversity. Anim. Genet. Resour. Inform. 25, 33–38.

103

Beriain, M.J., Horcada, A., Purroy, A., Lizaso, G., Chasco, J., Mendizabal, J.A., 2000. Characteristics of Lacha and Rasa Aragonesa lambs slaughtered at three live weights. J. Anim. Sci. 78, 3070–3077. Bray, A.R., Graafhuis, E., Chrystall, B.B., 1989. The cumulative effect of nutrition, shearing and preslaughter washing stresses on the quality of lamb meat. Meat Sci. 25, 59–67. Butterfield, R.M., Zamora, J., Thompson, J.M., Redichiffe, K.J., Griffiths, D.A., 1984. Changes in body composition relative to weight and maturity of Australian Dorset Horn rams and wethers. 1. Carcass muscle, fat, bone and organs. Anim. Prod. 39, 251–258. Castellana, E., Ciani, E., Cianci, D.,2008. La razza Leccese. In: La valorizzazione delle razze ovine autoctone dell’Italia Meridionale continentali. Adda Editore, Bari, Italy, pp. 147–160. Cecchi, F., Ciani, E., Castellana, E., Mazzanti, E., Ciampolini, R., 2008. The Leccese local sheep breed from Apulia (Italy): a questionnaire survey. In: Proc. 59th Annual Meeting of the European Association for Animal Production, 24–27 August 2008, Vilnius, Lithuania, N. 31, p. 64 (Abstract). Coro, F.A.G., Youssef, E.Y., Shimokomak, M., 2003. Age related changes in poultry breast meat collagen pyridinoline and texture. J. Food Biochem. 26, 533–541. D’Alessandro, A.G., Maiorano, G., Kowaliszyn, B., Loiudice, P., Martemucci, G., 2012. How the nutritional value and consumer acceptability of suckling lambs meat is affected by the maternal feeding system. Small Rumin. Res. 106, 83–91. Díaz, M.T., de la Fuente, J., Pérez, C., Lauzurica, S., Álvarez, I., Ruiz de Huido˜ bro, F., Velasco, S., Caneque, V., 2006. Body composition in relation to slaughter weight and gender in suckling lambs. Small Rumin. Res. 64, 126–132. Eastell, R., Lambert, H., 2002. Diet and healthy bones. Calcif. Tissue Int. 70, 400–404. Etherington, D.J., Sims, T.J., 1981. Detection and estimation of collagen. J. Sci. Food Agric. 32, 539–546. European Union, 1994. European Community Standard for the Classification of Light Lambs Carcasses, Brochure No. CM-84-94-703-ES-D. Publishing Bureau of the European Communities, L-2985 Luxembourg. ˜ Guía, E., Caneque, V., 1992. Crecimiento y desarrollo del cordero Talaverano. Evolución de las características que definen su canal. Investigación Agraria en Castilla-La Mancha. Serie: Area de Producción Animal, vol. 5. Juárez, M., Horcada, A., Al calde, M.J., Valera, M., Polvillo, O., Molina, A., 2009. Meat and fatty quality of unweaned lambs as affected by slaughter weight and breed. Meat Sci. 83, 308–313. Kemster, A.J., Croston, D., Guy, D.R., Jones, D.W., 1987a. Growth and carcass characteristics of crossbred lambs sired by ten sire breeds compared at the same estimated carcass subcutaneous proportion. Anim. Prod. 44, 83–98. Kemster, A.J., Croston, D., Guy, D.R., Jones, D.W., 1987b. Tissue growth and development in crossbred lambs sired by ten breeds. Livest. Prod. Sci. 16, 145–162. Lepetit, J., 2008. Collagen contribution to meat toughness: theoretical aspects. Meat Sci. 80, 960–967. Maiorano, G., Cavone, C., McCormick, R.J., Ciarlariello, A., Gambacorta, M., Manchisi, A., 2007. The effect of dietary energy and vitamin E administration on performance and intramuscular collagen properties of lambs. Meat Sci. 76, 182–188. Maiorano, G., Ciarlariello, A., Cianciullo, D., Roychoudhury, S., Manchisi, A., 2009. Effect of suckling management on productive performance, carcass traits and meat quality of Comisana lambs. Meat Sci. 83, 577–583. Maiorano, G., Filetti, F., Salvatori, G., Gambacorta, M., Bellitti, A., Oriani, G., 2001. Growth, slaughter and intra-muscular collagen characteristics in Garganica kids. Small Rumin. Res. 39, 289–294. Maiorano, G., Sobolewska, A., Cianciullo, D., Walasik, K., Elminowska˙ nska, ´ ´ A., Tavaniello, S., Zyli J., Bardowski, J., Wenda, G., Sławinska, Bednarczyk, M., 2012. Influence of in ovo prebiotic and synbiotics administration on meat quality of broiler chickens. Poult. Sci. 91, 2963–2969. Mancini, R.A., Hunt, M.C., 2005. Current research in meat color. Meat Sci. 71, 100–121. ˜ Martinez-Cerezo, S., Sanudo, C., Panea, B., Medel, I., Delfa, R., Sierra, I., Beltran, J.A., Cepero, R., Olleta, J.L., 2005. Breed, slaughter weight and ageing time effects on physicochemical characteristics of lamb meat. Meat Sci. 69, 325–333. Mazzone, G., Giammarco, M., Vignola, G., Sardi, L., Lambertini, L., 2010. Effects of rearing season on carcass and meat quality of suckling Apennine light lambs. Meat Sci. 86, 474–478. McCormick, R.J., 1994. The flexibility of the collagen compartment of muscle. Meat Sci. 36, 79–91.

104

A.G. D’Alessandro et al. / Small Ruminant Research 114 (2013) 97–104

McCormick, R.J., 1999. Extracellular modifications to muscle collagen: implications for meat quality. Poult. Sci. 78, 785–791. McCormick, R.J., 2009. Collagen. In: Du, M., McCormick, R.J. (Eds.), Applied Muscle Biology and Meat Science. CRC Press, London, UK, pp. 129–148. Morand-Fehr, P., Fedele, V., Decandia, M., Le Frileux, Y., 2007. Influence of farming and feeling systems on composition and quality of goat and sheep milk. Small Rumin. Res. 68, 20–34. Nishimura, T., 2010. The role of intramuscular connective tissue in meat texture. Anim. Sci. J. 81, 21–27. ˜ F., Cano, T., Domenech, V., Alcade, Ma.J., Martos, J., Garía-Martinez, Pena, A., Herrera, M., Rodero, E., 2005. Influence of sex, slaughter weight ˜ and carcass weight on “non-carcass” and carcass quality in Segurena lambs. Small Rumin. Res. 60, 247–254. Russo, V., Preziuso, G., Verita, P., 2003. EU carcass classification system: carcass and meat quality in light lambs. Meat Sci. 64, 411–416. Santos-Silva, J., Mendes, I.A., Bessa, R.J.B., 2002. The effect of genotype, feeding system and slaughter weight on the quality of light lambs. 1. Growth, carcass composition and meat quality. Livest. Prod. Sci. 76, 17–25. SAS, 2002. SAS/STAT 9.1 User’s Guide Version, 9th edition. SAS Institute Incorporated, Cary, NC. Siculella, L., Damiano, F., Priore, P., Gnoni, G.V., 2008. Genetic variability analysis of Apulia sheep breeds by using microsatellites. In: Proc. 53rd National Meeting of the Italian Society of Biochemistry and Molecular Biology (SIB), 23–27 September 2008, Riccione, Italy, N. 6.5 (Abstract). Skapetas, B., Sinapis, E., Hatziminaoulglou, J., Karalazos, A., Katanos, J., 2006. Effect of age at slaughter on carcass characteristics and carcass composition in lambs of mountain Greek breed. Czech J. Anim. Sci. 51, 311–317. ˇ ˇ Skrlep, M., Candek-Potokar, M., 2006. Pork color measurement as affected by bloom time and measurement location. J. Muscle Foods 18, 78–87.

Taylor, St.C.S., Murray, J.I., Thonney, M.L., 1989. Breed and sex differences among equally mature sheep and goats. 4. Carcass muscle, fat and bone. Anim. Prod. 49, 385–409. Teixeira, A., Batista, S., Delfa, R., Cadavez, V., 2005. Lamb meat quality of two breeds with protected origin designation. Influence of breed, sex and live weight. Meat Sci. 71, 530–536. Teixeira, A., Delfa, R., Treacher, T., 1996. Carcass composition and body fat depots of Galego Bragancano and crossbred lambs by Suffolk and Merino Precoce sire breeds. Anim. Sci. 63, 384–394. Velleman, S.G., Yeager, J.D., Krider, H., Carrino, D.A., Zimmerman, S.D., McCormick, R.J., 1996. The avian low score normal muscle weakness alters decorin expression and collagen crosslinking. Connect. Tissue Res. 34, 33–39. Vernon, R.G., 1981. Lipid metabolism in adipose tissue of ruminants. In: Christie, W.W. (Ed.), Lipid Metabolism in Ruminant Animals. Pergamon Press, Oxford, UK, pp. 279–362. Vicenti, A., Ragni, M., Colonna, M.A., Megna, V., Vonghia, G., 2002. Effects of lamb feeding with suckling feeds containing ␻-3-polyunsaturated fatty acids. 2. Chemical composition and fatty acid profile of lamb meat. In: Proc. 48th International Congress of Meat Science and Technology, 25–30 August 2002, Rome, Italy, pp. 1034–1035. Wood, J.D., 1990. Consequences for meat quality of reducing carcass fatness. In: Wood, J.D., Fisher, A.V. (Eds.), Reducing Fatness in Meat Animals. Elsevier Applied Science, London, UK, pp. 344–397. Woessner Jr., J.F., 1961. The determination of hydroxyproline in the tissue and protein samples containing small proportions of this amino acid. Arch. Biochem. Biophys. 93, 440–450. Wojtysiak, D., Kaczor, U., Poltowics, K., Krzysztoforski, K., 2010. The effects of sex and slaughter weight on muscle fibre characteristics and physico-chemical properties of lam longissimus thoracis muscle. Anim. Sci. Pap. Rep. 28, 61–69.