- CLA
conjugated linoleic acid
- FA
fatty acids
- VA
trans-vaccenic acid
- SCFA
rated Fatty Acids
- MCFA
Medium Chain Saturated Fatty Acids
- MUFA
Mono-Unsaturated Fatty Acids
- PUFA
Poly-Unsaturated Fatty Acids
- LCFA
Long Chain Saturated Fatty Acids
- S/U
Saturated/Unsaturated ratio
- α-LNA
α- linolenic
- LA
linoleic acid
The demand for organically produced food is increasing. This growth could be attributed to the increased consumer interest in organic products. There are two major motives for buying organic products: health aspects for the consumers themselves and environmental concern (Haward & Green, Reference Haward and Green2003; Green, Reference Green2004). In addition, but not less important, there are ethical issues, a major one being concern for animal welfare. So, there is no doubt that a large proportion of consumers relate organic production to healthier food, less harm to the environment and better animal welfare. In general, it seems that health aspect have become more important during the 1990s (Wier & Calverly, Reference Wier and Calverly1999). Looking at the health aspect, it is important to realize that the consumers are not primarily focusing on the “traditional” nutritive value of the food, but on the increase of some nutrients, which have beneficial effects on human health.
Ruminant milk contains a large number of fatty acids (FA) some of which are very important for human health including polyunsaturated fatty acids (PUFA) within the ω-3 (omega-3) FA group, vaccenic acid (VA) and conjugated linoleic acid (CLA). The ω-3 FA have been linked to improved neurological function (Contreras & Rapoport, Reference Contreras and Rapoport2002), protection against coronary heart diseases (Albert et al. Reference Albert, Oh, Whang, Manson, Chae, Stampfer, Willett and Hu2005; Djousé et al. Reference Djoussé, Arnett, Carr, Eckfeldt, Hopkins, Province and Ellison2005) and prevention of some forms of cancer (Saadatian-Elahi et al. Reference Saadatian-Elahi, Norat, Goudable and Riboli2004). Biomedical studies with animal models have demonstrated a variety of effects from CLA, including anticarcinogenic, antiatherogenic, antiobesity, immune system enhancement and antidiabetic (Corl et al. Reference Corl, Barbano, Bauman and Ip2003; Larsson et al. Reference Larsson, Bergvist and Wolk2005). The cis-9, trans-11 CLA in milk fat is the major isomer and it represents about 78–89% of the total CLA in sheep milk fat (Antogiovanni et al. Reference Antogiovani, Mele, Buccioni, Petacchi, Serra, Mellis, Cordeddu, Banni and Secchiari2004).
Milk and dairy products from certified organic dairy production systems have been reported to contain higher concentrations of cis-9, trans-11 CLA, α-linolenic (α-LNA) acid (the main ω-3 FA in milk) (Jahreis et al. Reference Jahreis, Fritsche and Steinhart1996; Bergamo et al. Reference Bergamo, Fedele, Iannibelli and Marzillo2003; Butler et al. Reference Butler, Nielsen, Slots, Seal, Eyre, Sanderson and Leifert2008; Prandini et al. Reference Prandini, Sigolo and Piva2009; Slots et al. Reference Slots, Butler, Leifert, Kristensen, Skibsted and Nielsen2009) and α-tocopherol and β-carotene (Bergamo et al. Reference Bergamo, Fedele, Iannibelli and Marzillo2003; Butler et al. Reference Butler, Nielsen, Slots, Seal, Eyre, Sanderson and Leifert2008) than high-input conventional production systems. However some other studies have reported no differences in cis-9, trans-11 CLA milk fat content between organic and conventional or extensive production systems (Toledo et al. Reference Toledo, Anders and Björck2002; Ellis et al. Reference Ellis, Innocent, Grove-White, Cripps and McLean2006). The contradictory results of these studies are probably related to different feeding strategies among these different production systems.
Although there are a number of studies on dairy cows, which have investigated the differences in milk FA profile between organic and conventional production systems, to our knowledge there is only one study on dairy goats (Tudisco et al. Reference Tudisco, Cutrignelli, Calabrò, Picolo, Bovera, Guglielmelli, Moniello and Infascelli2010). Further to that Zervas et al. (Reference Zervas, Koutsotolis, Theodoropoulos and Zabeli2000) and Pirisi et al. (Reference Pirisi, Piredda, Sitzia, Fois, Kyriazakis and Zervas2002) have reported comparison of milk yield and composition from organic and conventional dairy sheep under controlled feeding regimen. In the absence of data on compositional differences, the aim of this study was to determine whether there is a difference in chemical composition of milk, particularly in FA profile, with emphasis on cis-9, trans-11 CLA, between conventional and organic dairy sheep and goat farms in Greece.
Materials and Methods
One hundred and sixty two individual milk samples were collected from sixteen dairy sheep and goats farms all over Greece in January–February 2009 about three months after parturition. The milk samples were taken as percentage (10%) of the milked female animals of each flock/herd.
Four dairy sheep (CS) and four dairy goat (CG) farms were selected representing common conventional production and feeding systems in Greece. Another four dairy sheep (OS) and four dairy goat (OG) farms organically certified were selected representing organic production and feeding systems in Greece. Those organic farms produced milk according to the legislation concerning organic farming by the Greek Ministry of Rural Development and Food. The average flock/herd size was around 100 females.
The CS and CG farms were selected from those using concentrates from the same feed mill company in order to minimize the dietary effects. Then, in those areas OS and OG farms, with comparable size and management to the conventional ones, were also selected for this trial.
The nutrition of the CS and CG farms was based mainly on supplements, apart from the limiting grazing, during the winter months up to March–April. The CS supplement consisted of alfalfa hay, wheat straw and concentrates and that of CG of alfalfa hay and concentrates. The goats were grazing wooded pastures dominated by shrubs and trees, consisted of species such as Quercus coccifera, Pyrus amugdaliformis, Arbutus unedo, Spartum junceum, Phlomis fruticosa and Olea european.
The OS and OG animals were fed during the winter months with a mixed ration consisting of alfalfa hay and corn grain, grazing organic certified grasslands at the same time as the conventional.
The average concentrate composition was: maize grain (60%), barley grain (10%), soybean meal (15%), wheat middlings (10%), calcium phosphate and mineral and vitamins (5%).
All the detailed data concerning the sheep and goats farms used in this trial during the experimental period are presented in Table 1. The energy and crude protein (CP) intake from grazing (grass in the case of sheep or grass and shrubs in the case of goats) was calculated based on the assumption that those animals had certain energy and CP requirements for maintenance and milk production (Table 1), which were partly met by the supplementary feeding offered to them indoors, and partly by the grazed forage. Since the body condition score of the animals was rather constant (2·7 for the sheep and 2·5 for the goats in a scale from 1 to 5) during the experimental period, the estimated requirements met by grazing are based on the difference between actual total energy and CP requirements and those covered by supplementary feeding.
Table 1. Detailed data concerning the sheep and goats farms used in the experimental period.
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1 Grazing=Calculated by difference (energy and protein requirements based on maintenance and produced milk minus energy and CP covered by supplementary feeding)
2 Requirements of small ruminants (Zervas, Reference Zervas2007)
3 NEl=Net Energy of lactation
4 CP=Crude Protein
5 Calculated values=Calculated values from Tables: Zervas, (Reference Zervas2007)
6 Total regimen=Calculated energy, CP, etc coming from supplementary feeding+grazing in total
7 F/C=Forage /Concentrate ratio on a dry matter basis
8 +=According to balance calculations the grass intake by the conventional sheep should be very low as the animals covered their energy and CP requirements by the supplementary feeding
Milk and Feed samples analyses
Each milk sample was divided in two parts, one for chemical analysis and another for FA determination by gas chromatography, as described by Tsiplakou et al. (Reference Tsiplakou, Mountzouris and Zervas2006). Milk was analyzed for fat, protein, lactose, total solids (TS), and solids-not-fat (SNF), with IR spectrometry (Milkoscan 133/; Foss Electric, Hllerod, Demark), after appropriate calibration of the instrument according to Gerber (BSI, 1955), Kjeldahl (Inernational Dairy Federation (IDF), 1993) and chloramine-T method, respectively (IDF, 1964).
Feed samples (alfalfa hay, concentrates, corn grain, grass and shrubs) were analyzed for their FA profile (by gas chromatography) and chemical composition, as described by Tsiplakou et al. (Reference Tsiplakou, Mountzouris and Zervas2006) and Tsiplakou & Zervas (Reference Tsiplakou and Zervas2008) respectively.
Calculations for milk FA
Statistical analysis
The results are presented as least square means±sem. Farming system effects (CS vs. OS and CG vs. OG) on milk chemical composition and FA profile in each animal species was test by one-way ANOVA using SPSS statistical package (release 9.0.0). Post-hoc tests were performed using Duncan's multiple range test and significance was set at P<0·05.
Results
The data concerning the supplementary feeding of all sheep and goat farms and the calculated quantity of grass/shrubs intake, presented in Table 1, show that CS should have very low grass intake compared with the OS. The CG should also have lower grass and shrubs intake compared with the corresponding OG. However, in any case the grass/shrubs intake by goats was much higher than that of sheep. According to those calculations, which are very close to reality, based on the animal actual requirements and the known quantities of the supplementary feeding, the forage/concentrate (F/C) ratio was very similar between conventional and organic farmed animals for each animal species (Table 1).
Based also on the data of Table 1, the NDF and ADF content (% DM) of total regimen was higher in CS and CG compared with the corresponding OS and OG.
The mean chemical composition of all milk types is presented in Table 3. The CS milk showed higher fat and TS content compared with the OS, while the protein, lactose and SNF did not differ. In goats milk the only difference found was the higher milk fat content of the CG compared with OG.
Milk fatty acid profile, the values of S/U ratio, AI and Δ−9 desaturase indices evaluated in conventional and organic sheep and goats' milk fat are also presented in Table 3. The significantly higher values of milk FA between CS vs. OS and CG vs. OG are shown in bold.
Discussion
Different feeding regimens have different impacts on composition and/or functional properties of raw milk (Toledo et al. Reference Toledo, Anders and Björck2002). There are many sources of feeds like pasture, conserved forages (hay, silages, etc) and concentrates which are used in animal diets and different feeding strategies, which also affect, in different way, milk FA profile. An additional complicating factor when discussing effects of organic farming on food quality (e.g. FA profile of milk fat) is that organic production systems are not well-defined, but differ widely between countries, or in some cases even within the same country. In Denmark, for example, the conventional farms compared with the organic ones use different forages (Noziere et al. Reference Noziere, Graulet, Lucas, Martin, Groilier and Doreau2006), whereas in Sweden the feeding strategies between the two systems are very similar (Toledo et al. Reference Toledo, Anders and Björck2002). Taking into account that diet is the main factor which affects the milk FA profile, the direct comparison between organic and conventional production system is not easy (Sundrum, Reference Sundrum2001) and highlights the importance of repeated studies of sufficient sample size in different countries, to represent local management practices.
This study aimed to show the potential of the production system (organic vs. conventional) of dairy sheep and goats practiced in Greece to affect the composition of milk. The feeding system of dairy sheep and goats in Greece is based on seasonal (spring-early summer) natural grazing and on supplementary feeding (autumn-winter) which consists of home grown roughages (mainly alfalfa hay and straw) and concentrates (Zervas et al. Reference Zervas, Fegeros and Papadopoulos1996).
The type and the level of integration to be used depends on animal productivity, feedstuffs availability and milk price. Thus there is large variation among individual farms which makes the comparison of milk composition really difficult since it is well known that such a comparison should take into account the farm management system as well as seasonal and nutritional factors which are responsible for potential differences in milk FA profile. In this study, in order to avoid any confounding factors, the farms were selected to have comparable management, feeding per animal species and productive system. Ellis et al. (Reference Ellis, Innocent, Grove-White, Cripps and McLean2006) found that there was a significant effect of farming system (organic vs. conventional) in PUFA and ω-3 FA content of cows milk, even after accounting for some potentially confounding management and nutritional factors in the analyses.
Milk fat content of both OS and OG (Table 3) was significantly lower compared with the respective conventional. In the former study of Zervas et al. (Reference Zervas, Koutsotolis, Theodoropoulos and Zabeli2000) no difference in milk composition between organic and conventional dairy sheep was found, because their feeding regimen was controlled and comparable. The observed differences in milk fat content, in this study, between the two systems (conventional vs. organic) could be attributed to the lower NDF and ADF content of the OS and OG regimen compared with that of the conventional, which is the consequence of the higher grass or grass/shrubs intake by organically farmed sheep and goats respectively (Table 1). These results disagree with those of Pirisi et al. (Reference Pirisi, Piredda, Sitzia, Fois, Kyriazakis and Zervas2002) who found no differences in sheep milk composition between the two farming systems with the exception of higher casein production in conventional system and those of Tudisco et al. (Reference Tudisco, Cutrignelli, Calabrò, Picolo, Bovera, Guglielmelli, Moniello and Infascelli2010) who found significantly higher milk fat content in OG compared with the CG. However, significantly lower milk fat content has been observed in dairy cows in an organic, compared with a conventional farming system by Jahreis et al. (Reference Jahreis, Fritsche and Steinhart1996), but in that study only one organic farm was included.
The concentration of MCSFA in sheep and goats organic milk was significantly lower than the respective conventional samples (Table 3). A similar trend was observed for the SCSFA content but the difference was significant only in the goats' milk. The relatively higher pasture and shrubs intake that characterize sheep and goats reared in the organic farms respectively compared with the conventional farms (Table 1) could explain these differences. The higher content of unsaturated fatty acids in pasture and shrubs (Table 2) exert a potent inhibitor effect on the de novo synthesis of fatty acids at the mammary gland which is responsible for the decrease of SCSFA and MCSFA concentration in milk fat (Barber et al. Reference Barber, Clegg, Travers and Vernon1997).
Table 2. Chemical composition (g/kg dry matter) and the main fatty acids (% of total FA) of shrubs (n=6) and other feedstuffs (n=6)
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The significantly higher content of α-LNA in OS and OG milk compared with conventional milk is due to the higher pasture and shrubs intake mentioned earlier. On the other hand, the significantly higher LA concentration in CS milk compared with the OS milk, can be attributed to higher concentrate intake (Table 1).
The ω-6/ω-3 FA ratio was lower in OS compared with CS milk (Table 3), being closer to the suggested optimum ω-6/ω-3 FA ratio in the human diet of 1/1 (Simopoulos, Reference Simopoulos2002). These results agree with those of Ellis et al. (Reference Ellis, Innocent, Grove-White, Cripps and McLean2006) and Slots et al. (Reference Slots, Butler, Leifert, Kristensen, Skibsted and Nielsen2009) who reported lower ω-6/ω-3 ratio in organic milk of dairy cows. This lower ratio of the OS milk gives a higher nutritional value to milk, indeed, as described by Thorsdottir et al. (Reference Thordottir, Hill and Ramel2004) has been found a positive relationship between increasing milk ω-6/ω-3 FA ratio and the prevalence of type-2 diabetes and mortality due to coronary heart disease. Milk enriched with ω-3 FA favourably alters the plasma fat content, reducing the concentration of fatty acids associated with increased risk of cardiovascular disease (Baró et al. Reference Baró, Fonollá, Peña, Martínez-Férez, Lucena, Jiménez, Boza and López-Huertas2003; Carrero et al. Reference Carrero, Baró, Fonollá, González-Santiago, Martínez-Férez, Castillo, Jiménez, Boza and López-Huertas2004). However, there is a strong need of further investigations to verify a benefit to human health following consumption of low ω-6/ω-3 ratio.
Table 3. Chemical composition, FA profile (% of total FA) and Δ−9 desaturase indexes of conventional and organic sheep and goat milk fat (Mean±sem)
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1 CS=Conventional Sheep
2 OS=Organic Sheep
3 CG=Conventional Goats
4 OG=Organic Goats
Means with different superscripts (a and b) in the row for each parameter differ significantly (P⩽0·05)
VA is not included in the C18:1 content
The high variety of feeds used in dairy cows maybe responsible for the contradictory results concerning cis-9, trans-11 CLA milk fat content. Indeed, some researchers have observed significantly higher cis-9, trans-11 CLA in organic milk compared with the respective conventional (Jahreis et al. Reference Jahreis, Fritsche and Steinhart1996; Bergamo et al. Reference Bergamo, Fedele, Iannibelli and Marzillo2003; Butler et al. Reference Butler, Nielsen, Slots, Seal, Eyre, Sanderson and Leifert2008; Slots et al. Reference Slots, Butler, Leifert, Kristensen, Skibsted and Nielsen2009; Prandini et al. Reference Prandini, Sigolo and Piva2009) whereas some others found no differences (Toledo et al. Reference Toledo, Anders and Björck2002; Ellis et al. Reference Ellis, Innocent, Grove-White, Cripps and McLean2006) in dairy cows. To our knowledge there is no report on organic sheep milk FA profiles, in order to make comparison. Only in the study of Tudisco et al. (Reference Tudisco, Cutrignelli, Calabrò, Picolo, Bovera, Guglielmelli, Moniello and Infascelli2010) was significantly higher cis-9, trans-11 CLA milk fat content found in OG compared with the CG.
A significantly higher content of cis-9, trans-11 CLA was found in milk fat of the OS (Table 3) which could also be attributed to higher herbage intake, since herbage has high α-LNA (60% of the total FA) content (Cabiddu et al. Reference Cabiddu, Decandia, Addis, Piredda, Pirisi and Molle2005; Chilliard et al. Reference Chilliard, Glasser, Ferlay, Bernard, Rouel and Doreau2007). On the contrary, in goats' milk fat cis-9, trans-11 CLA content did not differ between OG and CG milk (Table 3) despite the fact that herbage or shrubs intake with higher PUFA content was higher in the organic goats (Table 1). The shrub intake by goats, which are rich in tannins, may inhibit rumen biohydrogenation and consequently the cis-9, trans-11 CLA production (Cabiddu et al. Reference Cabiddu, Molle, Decandia, Spada, Fiori, Piredda and Addis2009). In accordance with the results of this study, no significant differences on cis-9, trans-11 CLA content in goats' milk were observed by Tsiplakou et al. (Reference Tsiplakou, Mountzouris and Zervas2006) when the animals were kept indoors or outdoors (fed only herbage), or when the goats fed olive tree leaves with high α-LNA content (Tsiplakou et al. Reference Tsiplakou and Zervas2008). However, further to that, recent experimental data have shown that there are species differences between sheep and goats in their cis-9, trans-11 CLA milk fat content due to the differences in mRNA Δ−9 desaturase expression in their mammary gland, when the two animals species (sheep/goats) are fed with the same dietary treatments (Tsiplakou et al. Reference Tsiplakou, Flemetakis, Kalloniati, Papadomichelakis, Katinakis and Zervas2009).
The majority of cis-9, trans-11 CLA in milk fat is of endogenous origin, synthesized from VA via Δ−9 desaturase enzyme. The best indicator of Δ−9 desaturase activity is the C14:1/C14:0, because all C14:0 in milk fat is produced by de novo synthesis in the mammary gland, whereas the other acid substrates (C16:0 and C18:0) can be absorbed from the gut (Cabiddu et al. Reference Cabiddu, Decandia, Addis, Piredda, Pirisi and Molle2005). In agreement with Addis et al. (Reference Addis, Cabiddu, Pinna, Decandia, Piredda, Pirisi and Molle2005), C14:1/C14:0 and C16:1/C16:0 ratios, obtained in this study, in sheep and goats' milk fat in both production systems were lower than the other two Δ−9 desaturase ratios (Table 3) because only a small proportion of C14:0 and C16:0 is desaturated to C14:1 and C16:1 respectively (Chilliard et al. Reference Chilliard, Ferlay, Mansbridge and Doreau2000). A higher efficiency of Δ−9 desaturase activity was estimated in both animal species and both production systems on the basis of the ratio C18:1/C18:0 (Table 3). As matter of fact that C18:0 is the most preferred substrate of Δ−9 desaturase in the mammary gland (Chilliard et al. Reference Chilliard, Ferlay, Mansbridge and Doreau2000; Mosley & McGuire, Reference Mosley and McGuire2003).
Conclusions
The results of this study have shown that the production system of goat and sheep species, organic vs. conventional, as practiced in Greece has an impact on milk composition and FA profile. Organic milk is characterized by a higher nutritional value due to the higher amounts of MUFA, PUFA, α-LNA, cis-9, trans-11 CLA and ω-3 in sheep and α-LNA and ω-3 in goats in comparison with respective conventional milk.