Meat quality of lambs of indigenous dairy Greek breeds as influenced by dietary protein and gastrointestinal nematode challenge

MEAT SCIENCE Meat Science 76 (2007) 779–786 www.elsevier.com/locate/meatsci

Meat quality of lambs of indigenous dairy Greek breeds as influenced by dietary protein and gastrointestinal nematode challenge G. Arsenos a

a,*

, P. Fortomaris a, E. Papadopoulos b, D. Kufidis a, C. Stamataris a, D. Zygoyiannis a

Department of Animal Production, Ichthyology, Ecology and Protection of Environment, School of Veterinary Medicine, Aristotle University of Thessaloniki, P.O. Box 393, Aristotle University Campus, 54124 Thessaloniki, Greece b Department of Infectious and Parasitic diseases, Avian Medicine and Pathology, School of Veterinary Medicine, Aristotle University, 54124 Thessaloniki, Greece Received 4 April 2006; received in revised form 27 February 2007; accepted 28 February 2007

Abstract The effect of dietary protein and gastrointestinal (GI) parasitism on growth and meat quality of lambs was assessed using 60 animals. The lambs were randomly allocated to one of three treatment groups (n = 20): group A, which served as control, group B that was regularly treated with albendazole and group C, which was given supplementary feeding with dietary protein. The three groups of lambs grazed into a pasture (Lolium perenne), which was contaminated with L3 larvae of GI nematodes. Lamb growth and condition score were assessed at 21-day intervals. After 126 days grazing all lambs were slaughtered and their carcasses were assessed for conformation and fatness and their ultimate pH was measured. Four carcasses from each group were randomly selected for meat quality measurements including physical analysis as well as colour, moisture, total fat, protein content and fatty acid composition. Parasitic challenge was assessed by means of faecal egg counts of lambs, pasture larvae and numbers of adult nematodes in the GI tract of lambs at slaughter. Growth rate of group B was higher (P < 0.01) than that of group A and resulted in significantly (P < 0.01) heavier carcasses. The produced carcasses had similar fatness, but differed significantly (P < 0.05), in their conformation; carcasses of group C scored higher than either those of group B or group A, respectively. There was a significant difference in the colour attributes (L*) with group A being significantly lighter (P < 0.05) and in pH (P < 0.01); Group B had the highest values. Carcasses of group C had the highest (P < 0.05) amounts of intermuscular fat compared to those of group B and A, respectively. The proportion of C16:1n-7 and C18:2n-6 was higher (P < 0.05) in subcutaneous fat tissue whereas the proportion of C18:0 was higher (P < 0.05) in muscle tissue. In conclusion, the present results showed that the increased protein content in the diet of growing lambs, grazing on a pasture infected with GI nematode larvae, resulted in the production of acceptable carcasses.  2007 Elsevier Ltd. All rights reserved. Keywords: Growing lambs; Dietary protein; Gastrointestinal nematodes; Meat quality

1. Introduction Gastrointestinal (GI) parasitism with nematodes is the most common and costly production disease of ruminant production systems, i.e., associated with reduced nutrient utilization, growth rate and milk production. Following *

Corresponding author. Tel.: +30 23 10 999 988; fax: +30 23 10 999 892. E-mail address: [email protected] (G. Arsenos). 0309-1740/$ - see front matter  2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.meatsci.2007.02.022

the earlier suggestion by Mulligan (1972) that GI parasitism induces an increase in the loss of endogenous protein, Sykes and Coop (1976) stated that even sub-clinical infections with GI parasites could lead to a 50% reduction in growth at the same feed intake. The reason for such deficiency is the shift in protein synthesis away from the carcass towards the liver and alimentary tract causing a reduction in efficiency of ME utilization for growth (Sykes, 2000). There is now abundant evidence in the literature of different approaches to enable small ruminants to resist GI

780

G. Arsenos et al. / Meat Science 76 (2007) 779–786

parasitism (Coop, Huntley, & Smith, 1995; Knox & Steel, 1996, 1999; Niezen, Charleston, Hodgson, Mackay, & Leathwick, 1996; Sykes & Coop, 1976; Valderra´bano, Delfa, & Uriarte, 2002; Wallace et al., 1999; Waller, 1999). Host nutrition has been considered to be an important factor influencing the host-parasite relationship and improvements in nutrition, especially improving the metabolizable protein content of the diet is the most effective approach to reduce the dependence on anthelmintics in the control of GI parasitism (Van Houtert & Sykes, 1996; Sykes & Coop, 2001). The latter is important with regard to the anthelmintic resistance which is already relatively widespread in GI nematodes infecting sheep and goats (Coles, 2005; Papadopoulos, Himonas, & Coles, 2001) worldwide, as well as to the increased consumer demand for products from sustainable production systems (Sanu˜do, Sanchez, & Alfonso, 1998; Waller, 1999). An important question that has not been addressed is, to what extent does GI parasitism with nematodes affect the quality of the produced meat? The quality of the carcass has been the focus of our research for some years. Towards this aim we have been investigating the potential of indigenous Greek sheep breeds for meat production with heavier lamb carcasses than those traditionally produced in Greece (Zygoyiannis, Kyriazakis, Stamataris, Friggens, & Katsaounis, 1997) and the extent to which post-weaning nutrition could affect carcass composition at any defined body-weight or proportion of breed mature weight, acceptable to consumers (Zygoyiannis et al., 1999). As part of these investigations, the quality of the meat produced in terms of its cholesterol content (Arsenos, Zygoyiannis, Kufidis, Katsaounis, & Stamataris, 2000), the fatty acids composition (Arsenos, Kufidis, Zygoyiannis, Katsaounis, & Stamataris, 2006) as well as its eating quality and acceptability by consumer’s (Arsenos et al., 2002) have been reported. Recently, the epizootiology of GI parasitism in sheep and goat production systems in Greece has also been addressed (Papadopoulos et al., 2003; Papadopoulos, Arsenos, Coles, & Himonas, 2007). The objectives of this experiment were to assess the extent to which the performance of growing lambs as well as the quality of the meat produced and the fatty acid composition of muscle and fat tissue could be affected by GI nematodes and protein supplementation. 2. Materials and methods 2.1. Animal husbandry and experimental design A total of sixty (60) female lambs of the Karagouniko breed were used. The lambs at birth had a mean bodyweight (BW) of 4.3 ± 0.76 kg (mean ± SD) and standard husbandry procedures were applied at that point. Lambs were reared indoors with their dams until weaning at approximately 52 days of age when they had a mean BW of 14.4 ± 2.09 kg (mean ± SD). After weaning the lambs were kept indoors for a period that lasted 30 days. During

that time they were offered a ration of 250 g/head/day of a concentrate mixture containing 11.3 MJ ME/kg DM and 192 g CP/kg DM (Table 1) and 500 g/head/day of Lucerne (Trifolium reperns) hay. The experimental animals were vaccinated against clostridia (Covexin SCHERING-PLOUGH ANIMAL HEALTH). At the end of the indoor period and before turnout to grazing the lambs were allocated to one of three (3) treatment groups (A, B and C) of 20 animals each. The allocation into groups was balanced for body weight and body condition score (BCS) of lambs. The mean BW and BCS of lambs was 19.1 ± 2.04 kg and 2.6 ± 0.23 (mean ± SD), respectively. The turnout to pasture took place in mid-February. On the day of turnout (day 0) all animals were administered 5 mg/kg BW of albendazole (Albendazole VETERIN 600 mg bolus). A pasture of 2.2 ha of ryegrass (Lolium perenne), was used for grazing all the three groups of lambs. The average production of the pasture was about 2.500 kg DM/ha. The pasture contained 167 g CP/kg DM and 7.5 MJ ME/kg DM (mean values for the experimental period). The pasture was contaminated with L3 larvae of a mixture of GI nematodes. These larvae comprised various local sheep dominating genera originating from infected faecal material spread evenly on the pasture. The mass of faeces was about 6 kg/ha. The faecal egg count (FEC) of the faecal material was 500 and the genera composition was Teladorsagia 73%, Haemonchus 11%, Trichostrongylus 9%, Cooperia 1% and Chabertia/Bunostomum/ Oesophagostomum 6%. The contamination of the pasture was monitored by means of herbage larvae counts at the beginning of the experiment (day 0) and thereafter at 21day intervals (MAFF, 1986). The outdoor grazing period lasted 126 days for all lambs. During this period the lambs were housed overnight in a sheep shed with individual feeding facilities. Apart from grazing, the lambs were fed 100 g/ head/day of barley straw to avoid grass-scouring. The Table 1 Ingredients and chemical composition of the concentrate mixture used for lambs of groups A, B and C Ingredients (g/Kg dry matter) Ground barley Ground maize Soybean meal Wheat bran Mineral/vitamin premix

610 100 220 50 20

Component (g/Kg DM) Dry matter Crude protein Neutral detergent fibre Acid detergent fibre Acid hydrolysed ether extract Ash Calcium Phosphorus Metabolisable energy (MJ/Kg DM)*

891 192 246 106 28 74 07 06 11.3

* Metabolisable energy was estimated from apparent whole-tract digestibility measures made using sheep fed at maintenance.

G. Arsenos et al. / Meat Science 76 (2007) 779–786

experimental design involving the three groups of lambs was as follows: (i) lambs of group A (n = 20) served as controls (ii) lambs of group B received an anthelminthic treatment with Albendazole at 21-day intervals with the last treatment given after 84 days of the start of the trial. On the same days the animals of the two other groups were also administered with a placebo treatment, (iii) lambs of group C were offered a supplementary feed containing 20 g barley and 80 g of dietary protein (Hipro soya) per animal/day. The supplement contained 43.2 CP/kg DM and 13.3 MJ ME/kg DM and it was offered to individual lambs of each group every morning prior to turn out to pasture. After the lambs were turned out to pasture, FEC were monitored using the modified McMaster technique (MAFF, 1986), at 21-day intervals and composite coprocultures were performed for each of the group of animals. At the same time pasture larvae counts were measured in samples of the pasture herbage grazed by the lambs for assessing the parasitic challenge they faced at each time of sampling. At slaughter the GI tract of each animal was removed using standard necropsy procedures (MAFF, 1986). The removed GI tract was used for adult nematode counts and identification. 2.2. Growth, carcass and meat quality assessment The growth of lambs was assessed by recording BW and BCS at 21-day intervals. The lambs of all groups were slaughtered on day 126 after turnout to pasture. The lambs were transported for about 20 km to an EU registered slaughterhouse where they were electrically stunned before slaughtering. The weight of hot carcass was recorded to calculate killing out percentage (KOP). All carcasses were assessed for conformation (Regular, Ordinary, Poor) and fatness (Low, Slight, Average) and scored according to the EU standard scheme (European Commission Regulation No. 2137/1992), which is the common method in Greece. The carcasses were weighed (hot carcass weight) and kept for six hours at room temperature before refrigeration at +1 C for 24 h. Subsequently, the carcasses were re-weighed (cold carcass weight) and the ultimate pH (pHu) measured in the longissimus dorsi, using a portable pH-meter. Thereafter, four (4) carcasses from each group were randomly selected for further analyses. The selected carcasses were sawn down at the middle line through the centre of the vertebral column and the left hand side (LHS) of each carcass was used for dissection. They were dissected into lean, bone, subcutaneous fat, intermuscular fat and other tissues (nerves, tendons etc.). The dissected muscle and fat tissues were vacuum packed and stored at 30 C prior to subsequent meat quality assessment. Comprehensive meat quality measurements were made on four representative half-carcasses from each of the three experimental groups of lambs. Those included: (i) physical analysis as described by Fisher and deBoer (1994), (ii) CIE colour space was used to measure meat colour with a Min-

781

olta ChromaMeter, in the muscle longissimus dorsi, (iii) meat moisture, total fat, and protein content, (iv) fatty acid composition of muscle (composite sample of the dissected lean) and fat tissues (subcutaneous fat). The methodology for lipid extraction and fatty acids methyl esters preparation and analytical procedures were described in details by Arsenos et al. (2006). 2.3. Statistical analysis All statistical analyses were performed using Genstat version 5.3 (Lawes Agricultural Trust, 1993). One-way analysis of variance (ANOVA) was used to test for differences in all performance and carcass measurements between the three groups of lambs. Data were further analysed for the effects of different treatment on the three groups of lambs. Treatment was considered as the main plot and time was considered as sub-plot and hence changes in the BW of lambs during the grazing period were analyzed using a split-plot analysis of variance model. Growth rates (g/ day) of lambs during the grazing period, were estimated by linear regression, and analyzed using a one-way analysis of variance. The initial BW of lambs at turnout to pasture was used as a covariate in the above analyses where appropriate. A one-way analysis of variance was also used to test for differences between the three groups of lambs in terms of FEC and the numbers of L3 nematode larvae on pasture. Prior to analysis FEC and numbers of L3 nematode larvae were log transformed (log[v+1]) in order to stabilise variance and approximate normality. The transformed data are reported as back-transformed means. 3. Results 3.1. Lamb growth and carcass quality assessment The average BW of lambs at turnout to pasture and their final BW at slaughter, as well as their growth rate and carcass conformation for groups A, B, and C, respectively, are shown in Table 2. Growth rate of lambs of group B was higher (P < 0.01) than that of lambs of group A and resulted in significantly (P < 0.01) heavier carcasses. There were also significant differences (P < 0.01) in the condition score of lambs; lambs of group C had the highest condition score. The supplementary feeding of lambs of group C, with dietary protein and barley resulted in the fastest growth rate even compared with lambs treated with anthelmintics. The latter contributed to the significant interaction (P < 0.01) between time and group due to the fact that lambs in group A did not increase their BW to the same extent as those lambs of groups B and C during the grazing period (Fig. 1). However, there were no significant differences in weights of hot or cold carcasses between lambs of the three groups. The carcasses had similar fatness, but differed significantly (P < 0.05) in their conformation with those lambs of group C scoring higher than either those of lambs of group B or

782

G. Arsenos et al. / Meat Science 76 (2007) 779–786

Table 2 Lamb growth, carcass weight and carcass conformation, throughout the experimental period by group Performance

Group A (n = 20)

B (n = 20)

C (n = 20)

Initial body-weight (kg) Body-weight at slaughter (kg) Time taken (days) Daily BW gain (g) Body condition score (BCS) Hot carcass weight (kg) Cold carcass weight (kg) Killing out percentage (%) Carcass conformation Fatness pHua

19.0 35.6 126 132 2.70 17.2 16.6 47.1 2.3 2.15 5.53

19.3 37.5 126 144 2.77 17.4 17.2 47.7 2.5 2.15 5.60

19.1 39.3 126 158 2.91 18.4 18.0 48.5 2.8 2.30 5.54

a * ** ***

s.e.d.

Significance

0.65 1.02

NS

7.2 0.027 0.57 0.57 0.60 0.16 0.15 0.02

**

**

***

NS NS NS *

NS **

Ultimate pH measured at the longissimus dorsi of the left hand side carcass of lambs. P < 0.05. P < 0.01. P < 0.001.

slight fatness and were scored as either Regular (n = 24) or Ordinary (n = 20).

40 38

Group A

Group B

Group C

36

Live weight (kg)

34

3.2. Parasitic challenge

32 30 28 26 24 22 20 18 0

21

42

63

84

105

126

Days of grazing period

Fig. 1. Growth of experimental lambs during the grazing period by group. Results are means ± SE for 20 lambs per treatment.

A, respectively. Fig. 2 shows a frequency chart of the number of carcasses scored according to their conformation (Regular, Ordinary, Poor) and fatness (Low, Slight, Average). The overall majority of carcasses (44 out of 60) had

Fig. 3 shows the mean faecal egg counts (eggs/g of faeces) of lambs in the three groups. The screening of the faeces at the start of grazing revealed that all lambs were free of nematode eggs. Eggs appeared in faeces after 42 days grazing in all untreated animals and reached their maximum at 84 days. The mean FEC for lambs in group C remained significantly lower until day 105 after which there was an increase, but again the FEC were significantly lower than those of group A. Lambs in group B had very low parasitic burden up to day 84 when they were last drenched. Thereafter, there was a large rise in FEC of group B from day 105 to 126. Fig. 4 shows the average numbers of L3 nematodes identified in grass samples (per g DM of grass) of the pasture used for grazing of the three groups of lambs. The parasitic

Group A

Group B

Group C

12

12

11

10 8

7 66

6

5 4

4

2

2

1

2

2

1

1

0 R1

R2

R3

O1

O2

O3

P1

P2

P3

Classification

Feacal egg counts (eggs/g of faeces)

Frequencies (number of carcasses)

1000 14

900 Group A

Group B

Group C

800 700 600 500 400 300 200 100 0 0

21

42

63

84

105

126

Days of grazing period

Fig. 2. Frequency chart according to conformation (R: regular, O: ordinary, P: poor) and fatness (1: low, 2: slight, 3: average) of the carcasses of lambs by group.

Fig. 3. Mean faecal egg counts of experimental lambs during the grazing period by group. Results are means ± SE for 20 lambs per group.

Number of L3 Larvae per g DM of grass

G. Arsenos et al. / Meat Science 76 (2007) 779–786 Group A

Group B

Group C

45 40 35 30 25 20 15 10 5 0 0

21

42

63

84

105

126

783

darker colour compared to that of lambs of group A. There was a higher index of yellow in the meat of lambs of both B and C groups (b value increased), but such difference was not statistically significant. Following the dissection of the LHS of each carcass it was revealed that lambs in group C had the highest (P < 0.05) amounts of intermuscular fat compared to those of group B and A, respectively. Chemical analysis of carcasses showed that lamb carcass of group C had also the highest (P < 0.05) proportion of total fat (Table 3).

Days from start of grazing

3.4. Fatty acids in muscle and fat tissue Fig. 4. Variation of pasture contamination with L3 larvae during the grazing period. Results are means ± SE for 20 lambs per group.

challenge showed a peak by day 21 and then declined to moderate levels. The parasitic challenge was manifested to the same extent regarding the average numbers of adult worms found at necropsy of lambs of the three groups after slaughter (Fig. 5). There were no juveniles counted. As shown in Fig. 5, there were significant (P < 0.05) differences in the numbers of Teladorsagia spp ., Trichostrongylus spp., Haemonchus contortus and Chabertia spp.; lambs of group A had the highest numbers followed by group B and C, respectively. 3.3. Meat quality characteristics

40 35 30 Group A

Group B

Group C

25 20 15

4. Discussion The main objective was to investigate whether worm resistance and meat quality of lambs of indigenous dairy Greek breeds was influenced by dietary protein and GI nematode challenge. Effects of GI nematodes on meat quality is important considering the changes in small ruminant production systems, aimed at outdoor and organic systems, provided that meat quality and consumer acceptance are maintained (Arsenos, Banos, Valergakis, Fortomaris, & Zygoyiannis, 2004; Sanu˜do et al., 1998). As described in the Material and Methods Section the objectives were addressed by the use of three groups of lambs that were grazing in a pasture contaminated with L3 larvae of GI nematodes while they were subjected either to supplementary feeding with dietary protein sources (group B) or anthelminthic treatment (group C) or nothing (group A, control). 4.1. Lamb growth and carcass quality assessment

10 5

is ur

a rti be ha

Tr ic h

um C

os

to

om st

op ha g es

at em N

m

um

iru s od

pe oo C

Bu no

s

os

do Tr ic h

la

lu

ia ag

tro ng y

rs

ch on Te

m ae H

ria

0 us

Genera found at necropsy of lambs

As shown in Table 2 there was a significant difference (P < 0.01) in the pH values between carcasses of lambs from different groups with those of group B showing the highest values. Table 3 presents the mean values and standard errors of differences of means (s.e.d.) of further data regarding meat quality measurements collected from the left hand side of four lamb carcasses for each experimental group. There was a significant difference in the colour attributes (L*) with group A being significantly lighter (P < 0.05). The reduced values of L* in lambs of groups B and C (Table 3) suggest that they produced meat with

Fatty acid composition of muscle and fat tissue (percentage by weight of total fatty acid) of lambs of the three treatment groups are presented in Table 4. The fatty acid composition of both the muscle and the fat tissue was similar between the lambs of the three groups. However, significant differences were observed when comparisons for individual fatty acids were made between muscle and fat tissue. The proportion of C16:1n-7 and C18:2n-6 was higher (P < 0.05) in fat tissue whereas the proportion of C18:0 was higher (P < 0.05) in muscle tissue. Although there was a trend for increased proportions of C18:1n-9 in muscle as well as MUFA and PUFA in fat tissue, such differences were not significant possibly due to the relatively small number of samples (n = 4 per group).

Fig. 5. Variation of adult worms found at necropsy in the gastrointestinal tract of experimental lambs by group. Results are means ± SE for 20 lambs per group.

Although a number of different approaches have been engaged to enable small ruminants to resist GI parasitism (Coop et al., 1995; Knox & Steel, 1996, 1999; Niezen et al., 1996; Sykes & Coop, 1976; Valderra´bano et al., 2002; Waller, 1999) there is a remarkable scarcity of information as to what extent does GI parasitism with nematodes affect the quality of the meat produced. The results of the present study suggest that lamb growth

784

G. Arsenos et al. / Meat Science 76 (2007) 779–786

Table 3 Measurements, physical and chemical analysis of carcasses of experimental lambs by group Group

s.e.d

Significance

A (n = 4)

B (n = 4)

C (n = 4)

Carcass Measurements Left hand side weight before dissection (g) Kidney (g) KKCF a and pelvic fat (g) Ribeye length (mm)a Ribeye width (mm) Colour a* b* L*

8387 65.5 274.0 54.1 25.9 9.37 4.51 30.7

8475 60.0 278.5 54.5 27.6 10.03 5.75 29.1

8998 61.0 338 60.2 25.7 10.07 4.72 27.2

303.2 3.70 52.2 3.02 1.58 0.60 0.57 1.00

NS NS NS NS NS NS NS

Physical analysis (dissection) LHS Weightb (g) Muscle (g) Subcutaneous fat (g) Intermuscular fat (g) Bone (g) Other tissues (g)

8030 4670 621 890 1480 174

8091 4558 706 1049 1427 185

8559 4905 718 1137 1499 145

238 180 124 69 89 9.9

NS NS NS

Chemical analysis Moisture (%) Protein (%) Total fat (%) Ash (%)

72.05 19.85 6.16 1.02

71.94 19.99 6.30 1.03

72.18 19.81 6.47 1.02

1.20 1.02 0.09 0.06

NS NS

a b * **

*

*

NS **

*

NS

Kidney knob and channel fat. LHS weight after removal of KKCF and pelvic fat. P < 0.05. P < 0.01.

Table 4 Variation of fatty acid composition of intramuscular fat and adipose tissue in lambs, by group Group

s.e.d.

A

B

C

Location of adipose tissue a

C14:0 C16:0 C16:1n-7 C18:0 C18:1n-9 C18:2n-6 C18:3n-3 UFAc MUFA PUFA a b c * ***

Significance of:

b

IF (n = 4)

AT (n = 4) IF (n = 4)

AT (n = 4)

IF (n = 4)

AT (n = 4)

5.3 25.7 1.6 20.5 43.0 2.4 1.4 52.1 44.7 7.4

5.0 28.2 4.6 13.1 41.3 5.6 1.8 53.4 45.9 7.5

6.4 28.9 4.6 12.8 40.0 5.5 1.8 51.9 44.6 7.3

4.9 27.8 1.9 19.6 42.0 2.0 1.9 47.7 43.9 3.9

3.8 26.6 4.3 13.9 43.6 6.0 2.0 55.8 47.8 7.9

5.1 25.7 1.7 21.2 43.3 1.5 1.4 48.0 45.1 2.9

1.18 3.23 0.46 1.67 2.69 1.16 0.48 2.77 2.38 2.06

Group (G)

Location (L)

G·L

NS NS NS NS NS NS NS NS NS NS

NS NS

NS NS NS NS NS NS NS NS NS NS

*** ***

NS ***

NS *

NS *

Intramuscular fat extracted from the dissected lean. Subcutaneous fat. Unsaturated fatty acids. P < 0.05. P < 0.001.

and carcass weight at slaughter were positively affected by the supplementary feeding of dietary protein under the experimental conditions used; the outcome was in favour of the view that enhanced nutrition enables growing lambs to cope with GI nematode parasitism and the depression of the growth rate of lambs of group A, is in agreement

to the commonly held view about the effect of GI parasitism with nematodes on lamb growth (Sykes & Coop, 2001; Sykes & Greer, 2003). The results of the present study showed (Table 2) that lambs offered a dietary protein supplement maintained a higher daily growth rate compared to those of the control

G. Arsenos et al. / Meat Science 76 (2007) 779–786

group (group A), which is in agreement with the aforementioned previous studies on the ability of sheep to resist GI parasitism with nematodes. It is also interesting that the results of the present study suggest that lambs of all three groups, regardless of parasitism, managed to maintain a satisfactory level of productivity and approached their potential growth rate (Zygoyiannis et al., 1997). Moreover, the results suggest that there were no significant differences in the killing out percentage and the weight of the carcasses produced (Table 2). However, they indicated that carcass conformation was greatly affected by the different treatments; lambs of group A had the lowest scores. The latter is important because differences in conformation are likely to influence consumer preferences (Arsenos et al., 2002; Russo, Preziuso, & Verita, 2003; Sanu˜do et al., 1998). Throughout the experiment described here an effort was made to present the components that together account for the parasitic challenge faced by the experimental lambs. The results of faecal egg counts from lambs and the number of adult nematodes as well as those regarding the pasture larvae counts suggest that all lambs went through different levels of parasitic challenge. Lambs started to show moderate levels of eggs in their faeces only after day 42 after turn out to pasture; such levels are indicative of a significant adult worm population with associated damage to the GI tract. In our view the large rise in FEC of group B from day 105–126 (Fig. 4), is the result of the failure of those lambs to develop immunity because of continuous anthelmintic protection. Hence, when those lambs were exposed to the parasitic challenge without anthelmintic protection then they were infected heavily. The latter is most likely the reason why worm burdens did not differ between groups B and C. The fact that group B was last drenched at day 84 allowed considerable time (42 days) for the establishment of GIN infection. Moreover, an alternative suggestion is that the albendazole treatment was suppressing fecundity of established worms and so FEC in group B was lower but in the end worm counts were the same. 4.2. Meat quality characteristics and fatty acid composition The question, whether and to what extend the quality of meat produced as well as the fatty acid composition of muscle and fat tissues can be affected by parasitic challenge was also addressed in the experimental design. The results showed that the effects of nutritional management should be combined with the assessment of parasitic challenge in order to make objective judgements for the quality of lamb meat. Overall, the results suggest that lambs should be able to resist GI parasitism with nematodes based on supplementary feeding with dietary protein sources when grazing in pastures contaminated with moderate levels of GI nematode larvae. Hence, one of the conclusions of the present study is that supplementary feeding with dietary protein plays an important roˆle in fat deposition of lambs infected with GI parasites. Despite the fact that carcass weight was

785

similar between lambs of the three groups the intermuscular fat was significantly higher in lambs of groups B and C. Such differences are important with regard to the flavour of lamb meat and its eating quality (Arsenos et al., 2002; Santos-Silva, Mendes, & Bessa, 2002, 2003). The differences in the L* colour values, pH of meat, intermuscular fat and total fat content were the main findings regarding the assessment of meat quality characteristics (Tables 2 and 3). It should be noted here that the colour values of L* and a* are much lower when compared to those reported, for example by Russo et al. (2003), Santos-Silva et al. (2002,2003). Given that the above characteristics could influence the marketability of sheep meat we believe that it is important that the experimental design followed allowed for such a direct comparison. However, it is still unclear whether GI parasitism with nematodes or the treatment of animals of groups B and C account to the same or different degree to the changes in the colour of meat produced by the lambs used in the current experiment. The pH values were all in the normal range and unlikely to have any effect on quality. For example, when parasitic challenge varies from moderate to severe, any additional protein source to the infected animals may have different consequences for the quality of produced meat. The notion is that pH measurements in meat describe the progression of rigor mortis and the variation is often associated with variation in water holding capacity and muscle colour. One way of seeing this result is related to the acceptance of carcasses by consumers because meat colour is important to consumers and also the quantity and the quality of lipids within muscles have a substantial role in eating quality of meat (Arsenos et al., 2002). The profile of fatty acids between the three groups (Table 4) suggest that GI parasitism with nematodes is unlikely to induce any significant difference in the fatty acid composition, which was similar to that of previous studies using the same breed of lambs (Arsenos et al., 2006). Again the fact that the profile of fatty acids remained unchanged is important considering their role in the quality of produced meat (Wood et al., 2004). In conclusion, the results of this study emphasise the importance of coordinating parasite control programs with other aspects of flock management such as supplementary feeding with dietary protein. Acknowledgements The results described in this paper formed part of a wider series of studies that were financially supported by the European Commission (Project: FAIR3 CT 96-1485) as part of a collaborative programme between the UK, France, Greece and Spain. The Farmer Mr. Themistocles Zygoyiannis is greatly acknowledged for his assistance in animal and pasture management. We are also grateful to two anonymous referees and to the Associate editor of this journal, Dr. Mike Enser, for their extremely helpful comments on earlier drafts of the manuscript.

786

G. Arsenos et al. / Meat Science 76 (2007) 779–786

References Arsenos, G., Banos, G., Fortomaris, P., Katsaounis, N., Stamataris, C., Tsaras, L., et al. (2002). Eating quality of lamb meat: Effects of breed, sex, degree of maturity and nutritional management. Meat Science, 60, 379–387. Arsenos, G., Banos, G., Valergakis, G.E., Fortomaris, P., & Zygoyiannis, D. (2004). Proposed husbandry practices to ensure animal health and product quality in organic sheep and goat production systems. In: Proceedings of the 2nd SAFO Workshop (pp. 101–114). Germany: Witzenhausen. Arsenos, G., Kufidis, D., Zygoyiannis, D., Katsaounis, N., & Stamataris, C. (2006). Fatty acid composition of lambs of indigenous dairy Greek breeds of sheep as affected by post-weaning nutritional management and weight at slaughter. Meat Science, 73, 55–65. Arsenos, G., Zygoyiannis, D., Kufidis, D., Katsaounis, N., & Stamataris, C. (2000). The effect of breed slaughter weight and nutritional management on cholesterol content of lamb carcasses. Small Ruminant Research, 36, 275–283. Coles, G. C. (2005). Anthelmintic resistance – looking to the future: A UK perspective. Research in Veterinary Science, 78, 99–108. Coop, R. L., Huntley, J. F., & Smith, W. D. (1995). Effect of dietary protein supplementation on the development of immunity to Ostertagia circumcincta in growing lambs. Research in Veterinary Science, 59, 24–29. European Commission (1992). Community scale for the classification of carcasses of ovine animals. EEC council regulation No. 2137/92. European Commission, Brussels. Fisher, A. V., & deBoer, H. (1994). The EAAP standard method of sheep carcass assessment. Carcass measurements and dissection procedures. Livestock Production Science, 38, 149–159. Knox, M. R., & Steel, J. W. (1996). Nutritional enhancement of parasite control in small ruminant production systems in developing countries of south–east Asia and the Pacific. International Journal for Parasitology, 26, 963–970. Knox, M. R., & Steel, J. W. (1999). The effects of urea supplementation on production and parasitological responses of sheep infected with Haemonchus contortus and Trichostrongylus colubriformis. Veterinary Parasitology, 83, 123–135. Lawes Agricultural Trust (1993). Genstat 5 release 3.2 reference manual second edition. Oxford: Clarendon Press. MAFF, Ministry of Agriculture Fisheries and Food (1986). Manual of Veterinary Parasitological Laboratory Techniques. Reference Book 418, London. Mulligan, W. (1972). Effect of helminthic infection on protein metabolism of host. Proceedings of the Nutrition Society, 31, 47–51. Niezen, J. H., Charleston, W. A. G., Hodgson, J., Mackay, A. D., & Leathwick, D. M. (1996). Controlling internal parasites in grazing ruminants without recourse to anthelmintics: Approaches, experiences and prospects. International Journal for Parasitology, 26, 983–992. Papadopoulos, E., Arsenos, G., Coles, G. C., & Himonas, C. (2007). Gastrointestinal nematode infection pattern of Greek dairy goats reared under extensive husbandry conditions and treated with anthelmintics at different times during the year. Small Ruminant Research, 69, 68–73. Papadopoulos, E., Arsenos, G., Sotiraki, S., Deligiannis, C., Lainas, T., & Zygoyiannis, D. (2003). The epizootiology of gastrointestinal nema-

tode parasites in Greek dairy breeds of sheep and goats. Small Ruminant Research, 47, 193–202. Papadopoulos, E., Himonas, C., & Coles, G. C. (2001). Drought and flock isolation may enhance the development of anthelmintic resistance in nematodes. Veterinary Parasitology, 97, 89–93. Russo, C., Preziuso, G., & Verita, P. (2003). EU carcass classification system: Carcass and meat quality in light lambs. Meat Science, 64, 411–416. Santos-Silva, J., Bessa, R. J. B., & Mendes, I. A. (2003). The effect of supplementation with expanded sunflower seed on carcass and meat quality of lambs raised on pasture. Meat Science, 65, 1301–1308. 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. Livestock Production Science, 76, 17–25. Sanu˜do, C., Sanchez, A., & Alfonso, M. (1998). Small ruminant production systems and factors affecting lamb meat quality. Meat Science, 49, S29–S64. Sykes, A. R. (2000). Environmental effects on animal production: The nutritional demands of nematode parasite exposure. Asia–Australasian Journal of Animal Science, 13, 343–350. Sykes, A. R., & Coop, R. L. (1976). Intake and utilization of food by growing lambs with parasitic damage to small intestine caused by daily dosing with trichostrongylus colubriformis larvae. Journal of Agricultural Science, 86, 507–515. Sykes, A. R., & Coop, R. L. (2001). Interaction between nutrition and gastrointestinal parasitism in sheep. New Zealand Veterinary Journal, 49, 222–226. Sykes, A. R., & Greer, A. W. (2003). Effects of parasitism on the nutrient economy of sheep: An overview. Australian Journal of Experimental Agriculture, 43, 1393–1398. Valderra´bano, J., Delfa, R., & Uriarte, J. (2002). Effect of level of feed intake on the development of gastrointestinal parasitism in growing lambs. Veterinary Parasitology, 104, 327–338. Van Houtert, M. F. J., & Sykes, A. R. (1996). Implications of nutrition for the ability of ruminants to withstand gastrointestinal nematode infections. International Journal of Parasitology, 26, 1151–1167. Wallace, D. S., Bairden, K., Duncan, J. L., Eckersall, P. D., Fishwick, G., Holmes, P. H., et al. (1999). The influence of increased feeding on the susceptibility of sheep to infection with Haemonchus contortus. Animal Science, 69, 457–463. Waller, P. J. (1999). International approaches to the concept of integrated control of nematode parasites of livestock. International Journal for Parasitology, 29, 155–164. Wood, J. D., Richardson, R. I., Nute, G. R., Fisher, A. V., Campo, M., Kasapidou, E., et al. (2004). Effects of fatty acids on meat quality: A review. Meat Science, 66, 21–32. Zygoyiannis, D., Kyriazakis, I., Stamataris, C., Friggens, N. C., & Katsaounis, N. (1997). The growth and development of nine European sheep breeds. 2. Greek breeds: Boutsko, Serres and Karagouniko. Animal Science, 65, 427–440. Zygoyiannis, D., Katsaounis, N., Stamataris, C., Arsenos, G., Tsaras, L., & Doney, J. (1999). The use of nutritional management after weaning for the production of heavier lamb carcasses from Greek dairy breeds. Livestock Production Science, 57, 279–289.