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Effect of ewe's milk versus milk-replacer rearing on mineral composition of suckling lamb meat and liver
Small Ruminant Research 68 (2007) 296–302
Effect of ewe’s milk versus milk-replacer rearing on mineral composition of suckling lamb meat and liver Mar´ıa Teresa Osorio a , Jos´e Mar´ıa Zumalac´arregui a , Bel´en Bermejo a , Anastasio Lozano a , Ana Cristina Figueira b , Javier Mateo a,∗ a
Department of Food Hygiene and Technology, University of Le´on, Campus Vegazana s/n, 24071 Le´on, Spain b Escola Superior de Tecnologia, Universidade do Algarve, Campus da Penha, 8005-139 Faro, Portugal Received 18 April 2005; received in revised form 16 September 2005; accepted 29 November 2005 Available online 18 January 2006
Abstract The effect of ewe’s milk versus artificial rearing on the mineral content of suckling lambs muscle and liver was investigated, using a practically non-destructive sampling of carcasses. Mineral content was determined by inductively coupled plasma atomic emission spectroscopy (ICP-AES). Significant differences in mineral composition of muscle and liver were observed between the two groups belonging to each type of weaning. In muscle, these differences were mostly detected for Na, Zn and particularly Mn contents. As for the liver’s mineral content, significant higher concentrations of K, P and Cu and lower amounts of Zn and Mn were observed in samples from ewe’s milk reared lambs, when compared to those from hand reared ones. Results obtained lead to the conclusion that mineral composition of suckling lamb’s muscle and liver differed significantly according to the mineral intake of the ingested milk or formula. However, determination of the mineral content of either lambs’ muscle or liver does not seem to provide an accurate and sensible method for discriminating between carcasses from either type of rearing. © 2005 Elsevier B.V. All rights reserved. Keywords: Suckling lamb; Meat composition; Liver composition; Mineral elements; Milk-replacers
1. Introduction “Castilla y Le´on” is the Spanish region with the largest sheep stock (ca. 6 millions), from which approximately 2.5 millions are slaughtered annually for human consumption. Most of these (ca. 60–70%) are suckling lambs ‘lechales’ with ages between 25 and 45 days and with a carcass weight of less than 7 kg, coming from milk production systems (Sa˜nudo et al., 1998). The relevance and high edible quality of suckling lamb meat from Churra, Castellana and Ojalada breeds produced in the ∗
Corresponding author. Tel.: +34 987291247; fax: +34 987291284. E-mail address: [email protected] (J. Mateo).
0921-4488/$ – see front matter © 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.smallrumres.2005.11.010
‘Castilla y Le´on’ region has been recognised, and thus protected, by a geographical indication: PGI ‘Lechazo de Castilla y Le´on’ (Council Regulation 2081/92/EC). Usually, after a few-days feeding with the calostrum, suckling lambs either remain with their mothers to suckling the ewes’ milk or are reared with a milk-substitute. Apparently, rearing suckling lambs, with either type of feeding implies some differences, regarding economical aspects (P´erez et al., 2001), namely feed conversion and cost of feeding; meat quality (i.e. nutritional characteristics and eating quality) and animal welfare (De la Fuente et al., 1998; Sevi et al., 1999; Napolitano et al., 2002), supporting for either of those possibilities. Notwithstanding the possible advantages of milk-replacer rearing
M.T. Osorio et al. / Small Ruminant Research 68 (2007) 296–302
systems, in regulations of several lamb meat quality labels, as the PGI ‘Lechazo de Castilla y Le´on’ (Spain) – an European lamb meat quality label in which Churra is an authorised breed – it is required that suckling lambs are only fed with maternal milk, possibly to improve the last two aspects. Minerals are essential trace nutrients in humans and animals. Meat is an important source of several minerals, namely iron, zinc and phosphorus, in the occidental diet. Also, it is recognised that mineral content can be responsible for technological properties of meat, i.e. colour, tenderness and oxidation. Mineral contents of sheep and lamb tissues have been reported by several workers (Hazell, 1982; Ono et al., 1984; Krełowska-Kułas, 1992; Studzinski et al., 1992; Hoke et al., 1999; USDA, 2002; Hoffman et al., 2003; Sheridan et al., 2003). However, to our knowledge, information regarding suckling lambs could not be found to date. It has been reported in different experiments that mineral content of ovine (and of other animal species) tissues can vary considerably, and its concentration seems to be affected by genetic, physiological and environmental factors. Amongst non-genetic factors, the effect of dietary concentrations of elements and their chemical form, and the interactions with other nutrients have been the topics most researched (Wong-Valle et al., 1989; Medeiros et al., 1989; Pond, 1989; Grace and Lee, 1990; Ledoux et al., 1995; Sandoval et al., 1997; Pott et al., 1999; Reykdal and Thorlacius, 2001; Van Ravenswaay et al., 2001). In these cases, tissue accumulation of trace elements, namely Cu, Mo, Mn, Se, Zn, has been the main approach taken in explaining the observed variability on mineral content. Furthermore, the effect of growth promoters and hormones on mineral composition of ovine tissues has also been investigated (Gilka et al., 1989; Boila et al., 1990). In this sense, the aims of this study were, on the one hand to determine the mineral content of two suckling lamb tissues (muscle and liver). Additionally, to investigate potential differences in the concentration of minerals in those tissues between ewe’s milk and milk-replacer reared suckling lambs, using a practically non-destructive sampling of the carcasses, and then to evaluate the potential use of these differences to differentiate carcasses according the type of rearing. 2. Materials and methods 2.1. Samples A total of 65 carcasses of breast reared suckling lambs ‘lechales’ from a regional breed ‘Churra’ and another
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65 carcasses, from Churra ‘lechales’ hand reared with milk replacer, were randomly sampled in an industrial slaughterhouse during a 5 months period, and the mineral content of the antero-external part of the brachiocephalic muscle (ca. 20 g) was determined for these 130 carcasses. All carcasses used in the experiment originated from suckling lambs that were bred and reared in farms (25) affiliated to ANCHE–ANCHE is the biggest Churra breeders association in ‘Castilla y Le´on’ with 128 farms and 82,000 sheep –, and had a live weight range of 9–12 kg. Moreover, 10 of all those 65 muscle portions from each type of rearing where randomly chosen for determining their proximal composition. And finally, 10 livers from the 65 carcasses of suckling lambs reared with ewe’s milk and other 10 from the 65 animals reared with milk replacer were randomly collected for the determination of mineral content and proximate composition. Muscle and liver samples were homogenised and frozen at −40 ◦ C until the analysis were performed. In addition, samples of the five different commercial milk replacers used by ANCHE, were analysed. The proximate composition of the milk substitutes according to their labels, was: moisture, 4–5%; crude protein 23–24%; crude fat, 23–25%; ash, 6.6–8.6%; starch, 0–3%; crude fiber, 0–0, 5%; the ingredients: powdered milk and milk solids, vegetable fats and oils, products and subproducts from cereals, mineral supplements, i.e. iron and copper and Vitamins, i.e. E and A. 2.2. Nutritional analysis Moisture (ISO, 1973), fat (AOAC, 1999a) and protein (AOAC, 1999b) contents of muscle and liver were determined according to methods recommended by international organizations. Additionally, livers’ pH was determined potentiometrically. Regarding mineral content, duplicate aliquots of approximately 1 g (±0.01) of powdered-milk replacer, muscle or liver were accurately weighed, and digested with 10 mL of concentrated HNO3 in tightly closed screw cap glass tubes, for 12–18 h at room temperature and then for a further 4 h, at 90 ◦ C. Five millilitre of the mineralised solutions were diluted 1:2 (v/v) with deionised water for the analysis of Cu, Mn, Zn, Fe, Ca and Mg, or 1:10 (v/v) for the analysis of Na, K and P. Mineral content were determined by inductively coupled plasma atomic emission spectroscopy (ICP-AES) with a Perkin-Elmer Optima 2000 DV equipment. Instrument operating conditions were: radiofrequency power, 1400 W; plasma gas flow, 15.0 L/min; auxiliary gas flow, 0.2 L/min; nebulizer gas flow 0.75 L/min, crossed-flow;
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standard axial torch with 2.0 mm i.d. injector of silica; peristaltic pump flow, 1 mL/min; no. of replicates, 2. The spectrometer was calibrated for Cu, Mn, Zn, Fe, Ca and Mg determinations (at 224.7, 257.61, 213.9, 238.2, 393.4 and 279.6 nm, respectively) with nitric acid/water (1:1, v/v) standard solutions of 10 ppm of each element, and for Na, P and K (at 589.6, 213.6 and 766.5, respectively) with nitric acid/water (1:9, v/v) standard solutions of 30, 50 and 100 ppm, respectively. Viscosity effects were corrected using Sc as an internal standard, which was introduced into the plasma via an additional channel of the peristaltic pump. 2.3. Statistical analysis Statistical analyses were carried out using Statistica for Windows, release 5.1 Statsoft software. A one-way ANOVA design was performed, comparing each variable (mineral elements, moisture, fat and protein) between types of rearing. A principal component (PC) analysis was also performed, to obtain a better perception of differences between mineral composition of muscle and liver from carcasses for both types of rearing. In this PC analysis model, only the content of the mineral elements
showing significant differences between types of feeding by ANOVA (p < 0.05) were considered as variables. 3. Results Mineral composition of both muscle and liver samples from Churra suckling lamb carcasses are shown in Table 1. Significant differences in mineral composition of both tissues were observed between the two groups belonging to each type of weaning. In brachiocephalic muscle these differences were detected for Na, Zn (p < 0.01) and particularly Mn (p < 0.001) contents. Regarding the mineral content of liver, significant higher contents of K, P and Cu and lower contents of Zn and Mn were observed in samples from ewe’s milk reared lambs, when compared to those from hand reared ones. Although the statistical significance was always p < 0.05, the highest differences between means were detected for Cu, Zn and Mn. Results of the PC analysis for muscle and for liver are plotted in Figs. 1–4. In muscle, the two first PCs accounted for 68% of the variation (approximately 34% each one), whilst in liver they explained even more: 78%, with the first component accounting for 55% of the
Table 1 Mineral content (P, K and Na expressed as g 100 g−1 , others as mg 100 g−1 ) of brachiocephalic muscle (a) and liver (b) of carcasses from suckling lambs reared with ewe’s milk or milk-replacer Mineral
Ewe’s milk (n = 65)
Milk replacer (n = 65)
Significance
(a) Muscle K P Na
0.335 ± 0.025 0.209 ± 0.010 0.082 ± 0.010
0.338 ± 0.030 0.211 ± 0.014 0.076 ± 0.010
NS NS p < 0.01
21.3 ± 1.8 5.7 ± 0.9 3.3 ± 0.3 0.85 ± 0.20 0.081 ± 0.015 0.010 ± 0.003
2.1.7 ± 2.1 5.8 ± 1.9 3.1 ± 0.4 0.85 ± .0.26 0.079 ± 0.014 0.015 ± 0.005
NS NS p < 0.01 NS NS p < 0.001
Mineral
Ewe’s milk (n = 10)
Milk replacer (n = 10)
Significance
(b) Liver K P Na
0.349 ± 0.011 0.371 ± 0.018 0.088 ± 0.004
0.332 ± 0.016 0.353 ± 0.012 0.088 ± 0.004
p < 0.05 p < 0.05 NS
± ± ± ± ± ±
NS NS p < 0.05 NS p < 0.05 p < 0.05
Mg Ca Zn Fe Cu Mn
Mg Ca Zn Fe Cu Mn
20.24 7.6 4.4 4.37 5.77 0.30
NS, non-significant; p, probability level.
± ± ± ± ± ±
0.65 1.4 0.9 2.20 1.46 0.07
20.06 7.1 9.0 3.92 3.27 0.45
0.99 1.1 5.9 1.99 2.44 0.22
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Fig. 1. Projection, in the plane defined by the two first principal components, of the concentrations of the three mineral elements, Mn, Na and Zn, in muscle, used for the PC analysis.
Fig. 4. Projection, in the plane defined by the first two principal components, of the samples of muscle from carcasses of the two groups of rearing, based on its Cu, K, P, Mn and Zn concentrations.
Fig. 2. Projection, in the plane defined by the first two principal components, of the samples of muscle from carcasses of the two groups of rearing, based on its Mn, Na and Zn concentrations.
variation, and the second for 23%. Zn and Mn had the highest scores in the first PC in muscle (Fig. 1). Meanwhile, these two elements on the one side plus Cu on the opposite side were the minerals best describing the first PC in liver (Fig. 3). Na (positively), and P and K (both negatively) were the elements more related to principal component 2, respectively, in muscle and in liver (Figs. 1 and 3). Figs. 2 and 4 show that samples from each type of rearing are preferentially located in a different area of the respective plane. Thus, in muscle, ewe’s milk reared lambs samples are placed more to the upperright area, whilst in liver these are shifted towards the lower-left area. Table 2 Proximate composition (%) of brachiocephalic muscle (a) and pH and Proximate composition (%) of liver (b) of carcasses from suckling lambs reared either with ewe’s milk or milk-replacer Parameter
Fig. 3. Projection, in the plane defined by the two first principal components, of the concentrations of the five mineral elements Cu, K, Mn, P and Zn, in liver, used for the PC analysis.
Ewe’s milk (n = 10)
Milk replacer (n = 10)
Significance
(a) Muscle Moisture Protein Fat
72.5 ± 0.7 20.8 ± 0.6 4.8 ± 0.9
72.6 ± 0.6 20.9 ± 1.0 4.7 ± 1.3
NS NS NS
(b) Liver pH Moisture Protein Fat
6.26 72.2 18.9 4.7
NS, non-significant.
± ± ± ±
0.07 0.6 0.7 0.6
6.20 72.7 18.4 3.9
± ± ± ±
0.07 0.6 1.0 0.4
NS NS NS p < 0.01
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Table 3 Mineral content of commercial milk replacers, milk from Churra ewes, and from other breeds Milk replacersa (n = 5)
K (g kg−1 ) Ca (g kg−1 ) P (g kg−1 ) Na (g kg−1 ) Mg (g kg−1 ) Zn (mg kg−1 ) Fe (mg kg−1 ) Mn (mg kg−1 ) Cu (mg kg−1 )
Churra ewe’s milkb
Ewes’ milkc
Mean ± S.D.
Range
Mean ± S.D.
Range
2.38 ± 0.32 2.11 ± 0.40 1.40 ± 0.04 0.84 ± 0.14 0.22 ± 0.03 15.40 ± 6.13 6.82 ± 2.30 5.32 ± 2.79 <0.50
1.94–2.81 1.76–2.69 1.36–1.46 0.67–1.03 0.24–0.18 5.91–22.2 3.12–8.48 1.50–8.24 –
1.14 ± 0.06 1.85 ± 0.14 0.95 ± 0.09 0.68 ± 0.04 0.18 ± 0.01 ND 0.62 ± 0.07 ND 0.37 ± 0.05
1.40–1.96 0.92–2.59 1.01–1.57 0.27–0.65 0.14–0.21 0.50–5.54 0.66–0.86 0.08–0.36 0.05–1.76
ND, values not determined. a Results are expressed as in an aqueous solution; containing 20% (w/w) powdered milk replacer. b Pomar et al. (1999)—data obtained in our laboratories. c Assenat (1991).
The proximate composition of brachiocephalic muscle and liver are shown in Table 2. An analysis of these showed that no differences could be detected between muscles from each type of rearing. As for the liver, only fat content showed statistical differences, being higher in carcasses from breast reared lambs (p < 0.01). The mineral content of the milk replacers analysed is shown in Table 3, together with the mineral content data of ewe’s milk, which was reported in literatures (Assenat, 1991; Pomar et al., 1999). The amount of several elements, namely Zn, Fe and Mn, was clearly higher in milk replacers than in ewe’s milk. 4. Discussion Comparison of mineral content for suckling lamb muscle with data for muscle and lean of older lambs (Hazell, 1982; Ono et al., 1984; Gilka et al., 1989; Krełowska-Kułas, 1992; Hoke et al., 1999; USDA, 2002), revealed that the former appeared to have lower amounts of Ca, Fe and Cu than the latter, whilst similar amounts of the other elements, i.e. K, P, Na, Mg, Zn and Mn were observed. In average, roughly a two-fold difference in Fe and Cu contents, and even an almost three-fold in Ca were detected. Age could mostly account for these differences, which is evident in the case of Fe increasing with age, in animals for slaughterhouses. Ono et al. (1984) also found lower Ca and Fe contents (approximately 20% less), but not Cu, in lean of retail cuts of carcasses from 4 months old lambs, as compared to the respective lean from 8 months old lambs. The fact that hand-reared lambs’ muscle showed a 50% higher proportion of Mn might probably be due to milk replacers having a much higher Mn concentration
than ewe’s milk. Thus, tissue accumulation (even at this early age) could be one of the main causes for differences in Mn. However, no significant differences in the level of muscular Fe were observed in suckling lamb carcasses, in spite of the existing differences in Fe content between ewe’s milk and milk replacer. This fact could result from a scarce bioavailability of the Fe (FeSO4 ·7H2 O) added to milk replacers, when compared to the Fe of the milk. Grace and Lee (1990) also found that Fe intake due to FeSO4 ·7H2 O dietary supplementation did not affect the muscular Fe content in lambs. The amounts of mineral elements in samples of liver obtained from both types of rearing were within the ranges reported by other authors for ovine liver (Gilka et al., 1989; Pond, 1989; Studzinski et al., 1992; Reykdal and Thorlacius, 2001; Van Ravenswaay et al., 2001; USDA, 2002). However, Fe and Cu contents were at the lower end of those ranges. In contrast, Mn content of liver samples from milk-replacer rearing reached the upper ones. In the case of Zn and Mn, the differences observed might also be mostly explained by a variation in tissue accumulation, due probably to intake differences. Milk replacers had reasonably higher concentrations of Zn and Mn than ewes’ milk, therefore a higher intake of this elements could be expected for suckling lambs reared in this way. On the other hand, no differences could be detected for the dietary amount of Cu. In this case, the decrease in Cu content of liver – the major storage organ for Cu – when suckling lambs reared with milk-replacer were compared with those reared with ewe’s milk, could not be explained by a variation in intake. Thus, lower bioavailability of Cu in milk replacers, which are fortified with CuSO4 ·5H2 O, could account for differences in liver’s
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Cu content. Furthermore, according to Grace and Lee (1990), higher Fe intake in milk-replacer reared suckling lambs – milk replacer had a higher Fe content than ewe’s milk – could be another reason for lower Cu levels of those lambs’ livers. These authors stated as an important finding that a moderate increase in Fe intake could markedly reduce the Cu status of lambs. Regarding the PCA analysis, it was not possible to identify two clearly defined sets of results according to the type of rearing, neither for muscle, nor for liver samples. Furthermore, the samples of liver obtained from milk-replacer reared lambs seemed to subdivide into two separate groups of points (Fig. 4), one quite close to samples obtained from ewe’s milk reared lambs and other totally apart. This might be due to several differences in physico-chemical characteristics of the milk replacers used in feeding the lambs (namely osmolality and solubility). Another factor that should be taken into consideration is the potential variability in mineral composition of the water used for milk replacers’ reconstitution. These differences and their effect in mineral composition of lamb tissues seem to be an interesting subject to investigate in further research. 5. Conclusions Levels of Ca, Cu and Fe in suckling lamb meat appeared at concentrations roughly twice as low, when compared to meat from older lambs. The effects of feeding suckling lambs with ewe’s milk versus milk replacer on the means of several mineral contents of muscle and liver were identified. Differences were more pronounced in lamb’s liver, with Zn, Cu and Mn being the most affected elements. However, despite allowing for the detection of statistical differences, mineral analysis of muscle or liver does not seem to provide an accurate method for discriminating between carcasses from either rearing type. Acknowledgements The authors are grateful to ANCHE for providing the samples for analysis and to the Instrumental Techniques Laboratory of the University of Le´on, where the analysis with the ICP were carried out. This work has been financially supported by the “Junta de Castilla y Le´on” with FEDER funds. References AOAC, 1999a. Official method 991.36 fat (crude) in meat and meat products. In: Cunniff, P. (Ed.), Meat and Meat Products, vol. II. 16th
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ed., Official methods of analysis of the AOAC INTERNATIONAL, Gaithersburg, Maryland, pp. 3–4 (Chapter 39). AOAC, 1999b. Official method 981.10 crude protein in meat. Block digestion method. In: Cunniff. P. (Ed.), Meat and Meat Products, vol. II. 16th ed., Official methods of analysis of the AOAC INTERNATIONAL, Gaithersburg, Maryland, pp. 7–8 (Chapter 39). Assenat, L., 1991. Leche de oveja, composici´on y propiedades. In: Luquet, F.M. (Ed.), Leche y productos l´acteos, vol. 1. La leche de la mama a la lecher´ıa, Acribia. Zaragoza. Boila, R.J., Kennedy, A.D., Belluk, B.M., 1990. Effects of exogenous somatotropin on the concentration of minerals in the tissues of growing ram lambs. J. Anim. Sci. 68, 206–213. De la Fuente, J., Tej´on, D., Rey, A., Thos, J., L´opez-Bote, C.J., 1998. Effect of rearing system on growth, body compostion and development of digestive system in young lambs. J. Anim. Physiol. Anim. Nutr. 78, 75–83. Gilka, J., Jelinek, P., Jankova, B., Knesel, P., Krejci, V., Masek, J., Docekalova, H., 1989. Amino acid composition of meat, fatty acid composition of fat and content of some chemical elements in the tissues of male lambs fed monensin or lasaloid. Meat Sci. 25, 273–280. Grace, N.D., Lee, J., 1990. Effect of increasing Fe intake on the Fe and Cu content of tissues in grazing sheep. In: Proceedings of the New Zaeland Society of Animal Production, vol. 50, pp. 265–268. Hazell, T., 1982. Iron and zinc compounds in the muscle metas of beef, lamb, pork and chicken. J. Sci. Food Agric. 33, 1049–1056. Hoffman, L.C., Muller, M., Cloete, S.W.P., Schmidt, D., 2003. Comparison of six crossbred lamb types: sensory, physical and nutritional meat quality characteristics. Meat Sci. 65, 1265–1274. Hoke, I.M., Buege, D.R., Ellefson, W., Maly, E., 1999. Nutrient and related food composition of exported Australian lamb cuts. J. Food Composition Anal. 12, 97–109. ISO, 1973. Method R 1442. Moisture in Meat and Meat Products. International Organization for Standardization. Krełowska-Kułas, M., 1992. Study on some trace elements content of certain internal organs and muscles of lambs. Die Nahrung 36, 265–268. Ledoux, D.R., Pott, E.B., Henry, P.R., Ammerman, C.B., Merritt, A.M., Madison, J.B., 1995. Estimation of the relative bioavailability of inorganic copper sources for sheep. Nutr. Res. 15, 1803–1813. Medeiros, L.C., Russell, W.C., Stobart, R.H., Riley, M.L., West, S., 1989. Iron and zinc content of ovine muscle after dietary zincmethionine supplementation. Nutr. Rep. Int. 40, 509–516. Napolitano, F., Cifuni, G.F., Pacelli, C., Riviezzi, A.M., Girolami, A., 2002. Effect of artificial rearing on lamb welfare and meat quality. Meat Sci. 60, 307–315. Ono, K., Berry, B.W., Johnson, H.K., Russek, E., Parker, C.F., Cahill, V.R., Althouse, P.G., 1984. Nutrient composition of lamb of two age groups. J. Food Sci. 49, 1233–1257. P´erez, P., Maino, M., Morales, M.S., Soto, A., 2001. Effect of goat milk substitutes and sex on productive parameters and carcass composition of Creole kids. Small Ruminant Res. 42, 87–93. Pomar, E., Walser, N., Prieto, B., Tornadijo, M.E., Fresno, J.M., Gonz´alez, J., 1999. Chemical parameters and mineral composition of milk and whey in the manufacture of Zamorano D.O. Cheese. 4◦ Encontro de Qu´ımica dos Alimentos, Coimbra (Portugal), pp. 398–400. Pond, W.G., 1989. Effects of dietary protein level and clinoptilolite on the weight gain and liver mineral response of growing lambs to copper suplementation. J. Anim. Sci. 67, 2772–2781. Pott, E.B., Henry, P.R., Rao, P.V., Hinderberger, J., Ammerman, C.B., 1999. Estimated relative bioavailability of supplemental inorganic
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molybdenum sources and their effect on tissue molybdenum and copper concentrations in lambs. Anim. Feed Sci. Technol. 79, 107–117. Reykdal, O., Thorlacius, A., 2001. Cadmium, mercury, iron, copper, manganese and zinc in the liver and kidney of the Icelandic lamb. Food Addit. Contam. 18, 960–969. Sandoval, M., Henry, P.R., Littell, R.C., Cousins, R.J., Ammerman, C.B., 1997. Estimation of the relative bioavailability of zinc from inorganic zinc sources for sheep. Anim. Feed Sci. Technol. 66, 223–235. Wong-Valle, J., Henry, P.R., Ammerman, C.B., Rao, P.V., 1989. Estimation of the relative bioavailability of manganese sources for sheep. J. Anim. Sci. 67, 2409–2414. Sa˜nudo, C., Sanchez, A., Alfonso, M., 1998. Small ruminant production systems and factors affecting lamb meat quality. Meat Sci. 49 (Suppl. 1), S29–S64.
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Effect of ewe’s milk versus milk-replacer rearing on mineral composition of suckling lamb meat and liver Mar´ıa Teresa Osorio a , Jos´e Mar´ıa Zumalac´arregui a , Bel´en Bermejo a , Anastasio Lozano a , Ana Cristina Figueira b , Javier Mateo a,∗ a
Department of Food Hygiene and Technology, University of Le´on, Campus Vegazana s/n, 24071 Le´on, Spain b Escola Superior de Tecnologia, Universidade do Algarve, Campus da Penha, 8005-139 Faro, Portugal Received 18 April 2005; received in revised form 16 September 2005; accepted 29 November 2005 Available online 18 January 2006
Abstract The effect of ewe’s milk versus artificial rearing on the mineral content of suckling lambs muscle and liver was investigated, using a practically non-destructive sampling of carcasses. Mineral content was determined by inductively coupled plasma atomic emission spectroscopy (ICP-AES). Significant differences in mineral composition of muscle and liver were observed between the two groups belonging to each type of weaning. In muscle, these differences were mostly detected for Na, Zn and particularly Mn contents. As for the liver’s mineral content, significant higher concentrations of K, P and Cu and lower amounts of Zn and Mn were observed in samples from ewe’s milk reared lambs, when compared to those from hand reared ones. Results obtained lead to the conclusion that mineral composition of suckling lamb’s muscle and liver differed significantly according to the mineral intake of the ingested milk or formula. However, determination of the mineral content of either lambs’ muscle or liver does not seem to provide an accurate and sensible method for discriminating between carcasses from either type of rearing. © 2005 Elsevier B.V. All rights reserved. Keywords: Suckling lamb; Meat composition; Liver composition; Mineral elements; Milk-replacers
1. Introduction “Castilla y Le´on” is the Spanish region with the largest sheep stock (ca. 6 millions), from which approximately 2.5 millions are slaughtered annually for human consumption. Most of these (ca. 60–70%) are suckling lambs ‘lechales’ with ages between 25 and 45 days and with a carcass weight of less than 7 kg, coming from milk production systems (Sa˜nudo et al., 1998). The relevance and high edible quality of suckling lamb meat from Churra, Castellana and Ojalada breeds produced in the ∗
Corresponding author. Tel.: +34 987291247; fax: +34 987291284. E-mail address: [email protected] (J. Mateo).
0921-4488/$ – see front matter © 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.smallrumres.2005.11.010
‘Castilla y Le´on’ region has been recognised, and thus protected, by a geographical indication: PGI ‘Lechazo de Castilla y Le´on’ (Council Regulation 2081/92/EC). Usually, after a few-days feeding with the calostrum, suckling lambs either remain with their mothers to suckling the ewes’ milk or are reared with a milk-substitute. Apparently, rearing suckling lambs, with either type of feeding implies some differences, regarding economical aspects (P´erez et al., 2001), namely feed conversion and cost of feeding; meat quality (i.e. nutritional characteristics and eating quality) and animal welfare (De la Fuente et al., 1998; Sevi et al., 1999; Napolitano et al., 2002), supporting for either of those possibilities. Notwithstanding the possible advantages of milk-replacer rearing
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systems, in regulations of several lamb meat quality labels, as the PGI ‘Lechazo de Castilla y Le´on’ (Spain) – an European lamb meat quality label in which Churra is an authorised breed – it is required that suckling lambs are only fed with maternal milk, possibly to improve the last two aspects. Minerals are essential trace nutrients in humans and animals. Meat is an important source of several minerals, namely iron, zinc and phosphorus, in the occidental diet. Also, it is recognised that mineral content can be responsible for technological properties of meat, i.e. colour, tenderness and oxidation. Mineral contents of sheep and lamb tissues have been reported by several workers (Hazell, 1982; Ono et al., 1984; Krełowska-Kułas, 1992; Studzinski et al., 1992; Hoke et al., 1999; USDA, 2002; Hoffman et al., 2003; Sheridan et al., 2003). However, to our knowledge, information regarding suckling lambs could not be found to date. It has been reported in different experiments that mineral content of ovine (and of other animal species) tissues can vary considerably, and its concentration seems to be affected by genetic, physiological and environmental factors. Amongst non-genetic factors, the effect of dietary concentrations of elements and their chemical form, and the interactions with other nutrients have been the topics most researched (Wong-Valle et al., 1989; Medeiros et al., 1989; Pond, 1989; Grace and Lee, 1990; Ledoux et al., 1995; Sandoval et al., 1997; Pott et al., 1999; Reykdal and Thorlacius, 2001; Van Ravenswaay et al., 2001). In these cases, tissue accumulation of trace elements, namely Cu, Mo, Mn, Se, Zn, has been the main approach taken in explaining the observed variability on mineral content. Furthermore, the effect of growth promoters and hormones on mineral composition of ovine tissues has also been investigated (Gilka et al., 1989; Boila et al., 1990). In this sense, the aims of this study were, on the one hand to determine the mineral content of two suckling lamb tissues (muscle and liver). Additionally, to investigate potential differences in the concentration of minerals in those tissues between ewe’s milk and milk-replacer reared suckling lambs, using a practically non-destructive sampling of the carcasses, and then to evaluate the potential use of these differences to differentiate carcasses according the type of rearing. 2. Materials and methods 2.1. Samples A total of 65 carcasses of breast reared suckling lambs ‘lechales’ from a regional breed ‘Churra’ and another
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65 carcasses, from Churra ‘lechales’ hand reared with milk replacer, were randomly sampled in an industrial slaughterhouse during a 5 months period, and the mineral content of the antero-external part of the brachiocephalic muscle (ca. 20 g) was determined for these 130 carcasses. All carcasses used in the experiment originated from suckling lambs that were bred and reared in farms (25) affiliated to ANCHE–ANCHE is the biggest Churra breeders association in ‘Castilla y Le´on’ with 128 farms and 82,000 sheep –, and had a live weight range of 9–12 kg. Moreover, 10 of all those 65 muscle portions from each type of rearing where randomly chosen for determining their proximal composition. And finally, 10 livers from the 65 carcasses of suckling lambs reared with ewe’s milk and other 10 from the 65 animals reared with milk replacer were randomly collected for the determination of mineral content and proximate composition. Muscle and liver samples were homogenised and frozen at −40 ◦ C until the analysis were performed. In addition, samples of the five different commercial milk replacers used by ANCHE, were analysed. The proximate composition of the milk substitutes according to their labels, was: moisture, 4–5%; crude protein 23–24%; crude fat, 23–25%; ash, 6.6–8.6%; starch, 0–3%; crude fiber, 0–0, 5%; the ingredients: powdered milk and milk solids, vegetable fats and oils, products and subproducts from cereals, mineral supplements, i.e. iron and copper and Vitamins, i.e. E and A. 2.2. Nutritional analysis Moisture (ISO, 1973), fat (AOAC, 1999a) and protein (AOAC, 1999b) contents of muscle and liver were determined according to methods recommended by international organizations. Additionally, livers’ pH was determined potentiometrically. Regarding mineral content, duplicate aliquots of approximately 1 g (±0.01) of powdered-milk replacer, muscle or liver were accurately weighed, and digested with 10 mL of concentrated HNO3 in tightly closed screw cap glass tubes, for 12–18 h at room temperature and then for a further 4 h, at 90 ◦ C. Five millilitre of the mineralised solutions were diluted 1:2 (v/v) with deionised water for the analysis of Cu, Mn, Zn, Fe, Ca and Mg, or 1:10 (v/v) for the analysis of Na, K and P. Mineral content were determined by inductively coupled plasma atomic emission spectroscopy (ICP-AES) with a Perkin-Elmer Optima 2000 DV equipment. Instrument operating conditions were: radiofrequency power, 1400 W; plasma gas flow, 15.0 L/min; auxiliary gas flow, 0.2 L/min; nebulizer gas flow 0.75 L/min, crossed-flow;
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standard axial torch with 2.0 mm i.d. injector of silica; peristaltic pump flow, 1 mL/min; no. of replicates, 2. The spectrometer was calibrated for Cu, Mn, Zn, Fe, Ca and Mg determinations (at 224.7, 257.61, 213.9, 238.2, 393.4 and 279.6 nm, respectively) with nitric acid/water (1:1, v/v) standard solutions of 10 ppm of each element, and for Na, P and K (at 589.6, 213.6 and 766.5, respectively) with nitric acid/water (1:9, v/v) standard solutions of 30, 50 and 100 ppm, respectively. Viscosity effects were corrected using Sc as an internal standard, which was introduced into the plasma via an additional channel of the peristaltic pump. 2.3. Statistical analysis Statistical analyses were carried out using Statistica for Windows, release 5.1 Statsoft software. A one-way ANOVA design was performed, comparing each variable (mineral elements, moisture, fat and protein) between types of rearing. A principal component (PC) analysis was also performed, to obtain a better perception of differences between mineral composition of muscle and liver from carcasses for both types of rearing. In this PC analysis model, only the content of the mineral elements
showing significant differences between types of feeding by ANOVA (p < 0.05) were considered as variables. 3. Results Mineral composition of both muscle and liver samples from Churra suckling lamb carcasses are shown in Table 1. Significant differences in mineral composition of both tissues were observed between the two groups belonging to each type of weaning. In brachiocephalic muscle these differences were detected for Na, Zn (p < 0.01) and particularly Mn (p < 0.001) contents. Regarding the mineral content of liver, significant higher contents of K, P and Cu and lower contents of Zn and Mn were observed in samples from ewe’s milk reared lambs, when compared to those from hand reared ones. Although the statistical significance was always p < 0.05, the highest differences between means were detected for Cu, Zn and Mn. Results of the PC analysis for muscle and for liver are plotted in Figs. 1–4. In muscle, the two first PCs accounted for 68% of the variation (approximately 34% each one), whilst in liver they explained even more: 78%, with the first component accounting for 55% of the
Table 1 Mineral content (P, K and Na expressed as g 100 g−1 , others as mg 100 g−1 ) of brachiocephalic muscle (a) and liver (b) of carcasses from suckling lambs reared with ewe’s milk or milk-replacer Mineral
Ewe’s milk (n = 65)
Milk replacer (n = 65)
Significance
(a) Muscle K P Na
0.335 ± 0.025 0.209 ± 0.010 0.082 ± 0.010
0.338 ± 0.030 0.211 ± 0.014 0.076 ± 0.010
NS NS p < 0.01
21.3 ± 1.8 5.7 ± 0.9 3.3 ± 0.3 0.85 ± 0.20 0.081 ± 0.015 0.010 ± 0.003
2.1.7 ± 2.1 5.8 ± 1.9 3.1 ± 0.4 0.85 ± .0.26 0.079 ± 0.014 0.015 ± 0.005
NS NS p < 0.01 NS NS p < 0.001
Mineral
Ewe’s milk (n = 10)
Milk replacer (n = 10)
Significance
(b) Liver K P Na
0.349 ± 0.011 0.371 ± 0.018 0.088 ± 0.004
0.332 ± 0.016 0.353 ± 0.012 0.088 ± 0.004
p < 0.05 p < 0.05 NS
± ± ± ± ± ±
NS NS p < 0.05 NS p < 0.05 p < 0.05
Mg Ca Zn Fe Cu Mn
Mg Ca Zn Fe Cu Mn
20.24 7.6 4.4 4.37 5.77 0.30
NS, non-significant; p, probability level.
± ± ± ± ± ±
0.65 1.4 0.9 2.20 1.46 0.07
20.06 7.1 9.0 3.92 3.27 0.45
0.99 1.1 5.9 1.99 2.44 0.22
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Fig. 1. Projection, in the plane defined by the two first principal components, of the concentrations of the three mineral elements, Mn, Na and Zn, in muscle, used for the PC analysis.
Fig. 4. Projection, in the plane defined by the first two principal components, of the samples of muscle from carcasses of the two groups of rearing, based on its Cu, K, P, Mn and Zn concentrations.
Fig. 2. Projection, in the plane defined by the first two principal components, of the samples of muscle from carcasses of the two groups of rearing, based on its Mn, Na and Zn concentrations.
variation, and the second for 23%. Zn and Mn had the highest scores in the first PC in muscle (Fig. 1). Meanwhile, these two elements on the one side plus Cu on the opposite side were the minerals best describing the first PC in liver (Fig. 3). Na (positively), and P and K (both negatively) were the elements more related to principal component 2, respectively, in muscle and in liver (Figs. 1 and 3). Figs. 2 and 4 show that samples from each type of rearing are preferentially located in a different area of the respective plane. Thus, in muscle, ewe’s milk reared lambs samples are placed more to the upperright area, whilst in liver these are shifted towards the lower-left area. Table 2 Proximate composition (%) of brachiocephalic muscle (a) and pH and Proximate composition (%) of liver (b) of carcasses from suckling lambs reared either with ewe’s milk or milk-replacer Parameter
Fig. 3. Projection, in the plane defined by the two first principal components, of the concentrations of the five mineral elements Cu, K, Mn, P and Zn, in liver, used for the PC analysis.
Ewe’s milk (n = 10)
Milk replacer (n = 10)
Significance
(a) Muscle Moisture Protein Fat
72.5 ± 0.7 20.8 ± 0.6 4.8 ± 0.9
72.6 ± 0.6 20.9 ± 1.0 4.7 ± 1.3
NS NS NS
(b) Liver pH Moisture Protein Fat
6.26 72.2 18.9 4.7
NS, non-significant.
± ± ± ±
0.07 0.6 0.7 0.6
6.20 72.7 18.4 3.9
± ± ± ±
0.07 0.6 1.0 0.4
NS NS NS p < 0.01
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Table 3 Mineral content of commercial milk replacers, milk from Churra ewes, and from other breeds Milk replacersa (n = 5)
K (g kg−1 ) Ca (g kg−1 ) P (g kg−1 ) Na (g kg−1 ) Mg (g kg−1 ) Zn (mg kg−1 ) Fe (mg kg−1 ) Mn (mg kg−1 ) Cu (mg kg−1 )
Churra ewe’s milkb
Ewes’ milkc
Mean ± S.D.
Range
Mean ± S.D.
Range
2.38 ± 0.32 2.11 ± 0.40 1.40 ± 0.04 0.84 ± 0.14 0.22 ± 0.03 15.40 ± 6.13 6.82 ± 2.30 5.32 ± 2.79 <0.50
1.94–2.81 1.76–2.69 1.36–1.46 0.67–1.03 0.24–0.18 5.91–22.2 3.12–8.48 1.50–8.24 –
1.14 ± 0.06 1.85 ± 0.14 0.95 ± 0.09 0.68 ± 0.04 0.18 ± 0.01 ND 0.62 ± 0.07 ND 0.37 ± 0.05
1.40–1.96 0.92–2.59 1.01–1.57 0.27–0.65 0.14–0.21 0.50–5.54 0.66–0.86 0.08–0.36 0.05–1.76
ND, values not determined. a Results are expressed as in an aqueous solution; containing 20% (w/w) powdered milk replacer. b Pomar et al. (1999)—data obtained in our laboratories. c Assenat (1991).
The proximate composition of brachiocephalic muscle and liver are shown in Table 2. An analysis of these showed that no differences could be detected between muscles from each type of rearing. As for the liver, only fat content showed statistical differences, being higher in carcasses from breast reared lambs (p < 0.01). The mineral content of the milk replacers analysed is shown in Table 3, together with the mineral content data of ewe’s milk, which was reported in literatures (Assenat, 1991; Pomar et al., 1999). The amount of several elements, namely Zn, Fe and Mn, was clearly higher in milk replacers than in ewe’s milk. 4. Discussion Comparison of mineral content for suckling lamb muscle with data for muscle and lean of older lambs (Hazell, 1982; Ono et al., 1984; Gilka et al., 1989; Krełowska-Kułas, 1992; Hoke et al., 1999; USDA, 2002), revealed that the former appeared to have lower amounts of Ca, Fe and Cu than the latter, whilst similar amounts of the other elements, i.e. K, P, Na, Mg, Zn and Mn were observed. In average, roughly a two-fold difference in Fe and Cu contents, and even an almost three-fold in Ca were detected. Age could mostly account for these differences, which is evident in the case of Fe increasing with age, in animals for slaughterhouses. Ono et al. (1984) also found lower Ca and Fe contents (approximately 20% less), but not Cu, in lean of retail cuts of carcasses from 4 months old lambs, as compared to the respective lean from 8 months old lambs. The fact that hand-reared lambs’ muscle showed a 50% higher proportion of Mn might probably be due to milk replacers having a much higher Mn concentration
than ewe’s milk. Thus, tissue accumulation (even at this early age) could be one of the main causes for differences in Mn. However, no significant differences in the level of muscular Fe were observed in suckling lamb carcasses, in spite of the existing differences in Fe content between ewe’s milk and milk replacer. This fact could result from a scarce bioavailability of the Fe (FeSO4 ·7H2 O) added to milk replacers, when compared to the Fe of the milk. Grace and Lee (1990) also found that Fe intake due to FeSO4 ·7H2 O dietary supplementation did not affect the muscular Fe content in lambs. The amounts of mineral elements in samples of liver obtained from both types of rearing were within the ranges reported by other authors for ovine liver (Gilka et al., 1989; Pond, 1989; Studzinski et al., 1992; Reykdal and Thorlacius, 2001; Van Ravenswaay et al., 2001; USDA, 2002). However, Fe and Cu contents were at the lower end of those ranges. In contrast, Mn content of liver samples from milk-replacer rearing reached the upper ones. In the case of Zn and Mn, the differences observed might also be mostly explained by a variation in tissue accumulation, due probably to intake differences. Milk replacers had reasonably higher concentrations of Zn and Mn than ewes’ milk, therefore a higher intake of this elements could be expected for suckling lambs reared in this way. On the other hand, no differences could be detected for the dietary amount of Cu. In this case, the decrease in Cu content of liver – the major storage organ for Cu – when suckling lambs reared with milk-replacer were compared with those reared with ewe’s milk, could not be explained by a variation in intake. Thus, lower bioavailability of Cu in milk replacers, which are fortified with CuSO4 ·5H2 O, could account for differences in liver’s
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Cu content. Furthermore, according to Grace and Lee (1990), higher Fe intake in milk-replacer reared suckling lambs – milk replacer had a higher Fe content than ewe’s milk – could be another reason for lower Cu levels of those lambs’ livers. These authors stated as an important finding that a moderate increase in Fe intake could markedly reduce the Cu status of lambs. Regarding the PCA analysis, it was not possible to identify two clearly defined sets of results according to the type of rearing, neither for muscle, nor for liver samples. Furthermore, the samples of liver obtained from milk-replacer reared lambs seemed to subdivide into two separate groups of points (Fig. 4), one quite close to samples obtained from ewe’s milk reared lambs and other totally apart. This might be due to several differences in physico-chemical characteristics of the milk replacers used in feeding the lambs (namely osmolality and solubility). Another factor that should be taken into consideration is the potential variability in mineral composition of the water used for milk replacers’ reconstitution. These differences and their effect in mineral composition of lamb tissues seem to be an interesting subject to investigate in further research. 5. Conclusions Levels of Ca, Cu and Fe in suckling lamb meat appeared at concentrations roughly twice as low, when compared to meat from older lambs. The effects of feeding suckling lambs with ewe’s milk versus milk replacer on the means of several mineral contents of muscle and liver were identified. Differences were more pronounced in lamb’s liver, with Zn, Cu and Mn being the most affected elements. However, despite allowing for the detection of statistical differences, mineral analysis of muscle or liver does not seem to provide an accurate method for discriminating between carcasses from either rearing type. Acknowledgements The authors are grateful to ANCHE for providing the samples for analysis and to the Instrumental Techniques Laboratory of the University of Le´on, where the analysis with the ICP were carried out. This work has been financially supported by the “Junta de Castilla y Le´on” with FEDER funds. References AOAC, 1999a. Official method 991.36 fat (crude) in meat and meat products. In: Cunniff, P. (Ed.), Meat and Meat Products, vol. II. 16th
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