Fatty acid composition of muscle and internal fat depots of organic and conventional Payoya goat kids

Interest in the preservation of autochthonous breeds such as the Payoya goat (dairy breed), raised using extensive or semi-extensive grazing, has also recently increased among Spanish farmers. A study of the possibilities of transformation to organic production needs to analyze the quality of their products, specially the suckled kids. The objective of this study was to evaluate the fatty acid (FA) composition of Payoya goat kids under organic and conventional grazing–based management system. Forty-eight goat kids were selected (12 males and 12 females from each management system). The FA profile was determined in the Longissimus thoracis muscle, kidney and pelvic fat. Few gender differences were observed in the muscle and in the fat depots. The ratios of C14:0, C18:1 trans-11(VA), and several n-3 FA were higher in organic kid meat than in conventionally reared kid meat. Conventional kid fat depots have presented higher percentage of conjugated linoleic acid (CLA), lower CLA desaturase index, lower percentage of n-3 polyunsaturated fatty-acid (PUFA) and, consequently, higher n6:n3 PUFA ratio than organic kids. In conclusion, signif icant differences were found only in some FA percentages of muscle and adipose tissues of suckling kids raised in organic and conventional livestock production systems, probably due because the dams, in both experimental farms, were raised with similar semi-extensive system based on the grazing of natural pastures. Due to this reason, conventional grazing-based management farms could easily be transformed into organic production facilities. Additional key words: Payoya goat; CLA; n-3 fatty acids; meat; organic livestock production. * Corresponding author: pertinez@us.es Received: 03-12-12. Accepted: 11-07-13. Abbreviations used: ARA (arachidonic acid); CLA (conjugated linoleic acid); DHA (docosahexaenoic acid); EPA (eicosapentaenoic acid); FA (fatty acid); GLM (general linear model); MUFA (monounsaturated fatty acids); PUFA (polyunsaturated fatty acids); RA (rumenic acid); SFA (saturated fatty acids); UFA (unsaturated fatty acids); VA (vaccenic acid). Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA) Spanish Journal of Agricultural Research 2013 11(3): 759-769 Available online at www.inia.es/sjar ISSN: 1695-971-X http://dx.doi.org/10.5424/sjar/2013113-3808 eISSN: 2171-9292


Introduction
According to the European Union Directive (EC834/ 2007;EC, 2007) an organic animal production system should comply with the following requirements: contribute to the equilibrium of agricultural systems integrated with the natural environment, contribute to sustainable agriculture development, minimize all types of contamination, respect animal well-being, avoid systematic use of chemically synthesized substances, and renounce to the use of genetically modified organisms.
In the European Union, Spain has the second highest goat head number (2.6 million) and Andalusia (in southern Spain) is the region with major census (35.7% of the national total) (MAGRAMA, 2012) and also with the highest number (398) of goat herd organic farms (65% of the national total); of which 375 are meat production farms and 23 are dairy farms (MA-GRAMA, 2011).Interest in the preservation of autochthonous breeds, raised using extensive or semi-extensive grazing, has also recently increased among Spanish farmers and many of these breeds, such as the Payoya goat, are considered as special protection breeds (BOE, 2006).
Converting these breeds to organic production should be straightforward owing to the adaptive capacity and disease resistance of autochthonous breeds and to the rustic environment and nutritional resources available in mountain zones of Andalusía.According to organic production system requirements, mountain goat systems, in which feeding is largely based on grazing (Ruiz et al., 2008), could fairly easily be transformed into organic production (Mena et al., 2009a,b).A study of the possibilities of transformation to organic production needs to analyze, not only the technical and economical viability of the organic production systems, but also the quality of their products, specially the suckled kids.
The majority of goat farms raising the Payoya breed are located in the Sierra Norte of Cádiz (Andalucía, Spain).This breed is not as important economically or in census terms as the Malagueña or the Murciano-Granadina ones, but it is the one that best represents dairy goat production linked to grazing.The main objective of these farms is the yield marketable milk, and secondly the meat, for which kids must weigh 8-9 kg at slaughter.The reduced live weight at slaughter is due, on the one hand, to the fact that, if the weight is higher quickly it depreciates its economic value and, on the other hand, because the farmers want to take advantage of the productive potential milk faster (Mena et al., 2005).
Manipulation of dietary fatty acids (FA) is common because of the impact of FA intake on human health (MacRae et al., 2005).Myristic and palmitic acids are considered to negatively impact health, whereas conjugated linoleic acid (CLA) and polyunsaturated FA (PUFA), especially those of the n-3 series, are considered to be beneficial to human health; healthful FA benefit the cardiovascular system and lipid metabolism and may help to prevent cancer (MacRae et al., 2005).
Although gender effects on the FA content of goat meat and fat depots have been studied (Johnson et al., 1995;Mahgoub et al., 2002;Todaro et al., 2004;Santos et al., 2007;Nudda et al., 2008), the fatty acid composition of muscle and internal fat depots of goat kids under organic grazing-based management systems is not known.
The objective of this study was to evaluate the comparative fatty acid composition of muscle and internal fat depots of Payoya goat kids under organic and conventional grazing-based livestock production system.

Study area, experimental farm goats and kids
All goats utilized in this study were of the Payoya breed and located in the Sierra Norte of Cádiz (Andalucía, Spain).There are four organic and twenty seven conventional farms currently working with this breed (Association of Payoya Breeders, unpublished data).To evaluate the technical and economical viability of organic and conventional dairy goat farms of the Andalusian mountains and analyze the transition from conventional to organic production, 18 farms (14 conventional; 4 organic) were selected in collaboration with the Association of Payoya Breeders (Mena et al., 2009a,b).Within those farms and for the present study, one farm from each management system (certified organic under EC 834/2007834/ (EC, 2007) ) and conventional) was selected.Care and management of goats and kids was in accordance with Spanish Animal Welfare Act 32/2007 (BOE, 2007).
The dams in both experimental farms were raised with similar semi-extensive system based on the grazing of natural pastures (Ríos-Castaño, 2008;Mena et al., 2009a).The systems are characterized by a large land surface per animal, few sanitary problems, and grazing as an integral part of animal feeding, and the main difference is the major consumption of concentrates per animal and year in the conventional farm.In this sense and according to the previous technical characterization of the farms (Ríos- Castaño, 2008), a supplementary feed concentrate was added at a flat rate of 1.0 kg head -1 d -1 for the conventional farm and at 0.5 kg head -1 d -1 (organic constituents) for the organic farm (Table 1).On the rangeland, the diet was composed of herbaceous plant species and leaves and stems from Mediterranean shrubs and trees (mainly Mirtus communis, Pistacia lentiscus, Quercus ilex, Cistus salvifolius and Arbutus unedo).
Twenty-four goat kids of twin births (12 males and 12 females) born in October were selected from each farm (n = 48, 24 for each farm).The kids had free access to suckling 18-20 hours a day.The feedstuff usually is given in the milking parlour, thus goat kids did not have access to the concentrate.

Slaughter, muscle and adipose tissues sampling
All goat kids were slaughtered at a body commercial weight of 8.40 ± 0.06 kg at the Huelva municipality slaughterhouse after 16.33 ± 0.12 hours of fasting with free water access.After slaughter, carcasses were chilled at 4°C for 24 h and then the left half of each carcass was removed according to the procedure of  74), wheat husk (5), green pea (5), wheat bran (4), carob (4), sunflower seed (5), calcium carbonate (2.5), salt (0.5). c SFA, saturated fatty acids; MUFA, monounsaturated fatty acids; PUFA, polyunsaturated fatty acids.Colomer-Rocher et al. (1987) and transported under temperature for refrigeration to Huelva University.
Prior to dissection on the left half of carcass, the pelvic and kidney fats were removed; vacuum packed and frozen at -20°C until analysis.After the rib joints was obtained, the Longissimus thoracis were dissected, vacuum packed and frozen at -20°C until analysis.

Fatty acid composition
After thawing the Longissimus thoracis and pelvic and kidney fats, total FA were extracted, methylated and analyzed as described by Aldai et al. (2006).Fattyacid methyl esters were quantified with an Agilent 6890N gas chromatograph (Agilent Technologies Spain, S.L., Madrid, Spain) equipped with a flame ionization detector, an HP 7683 automatic sample injector, and an HP-88 J&W fused silica capillary column (100 m, 0.25 mm i.d., 0.2 µm film thickness; Agilent Technologies Spain, S.L.).Nonadecanoic acid methyl ester (C19:0 methyl ester; 10 mg mL -1 ) was used as an internal standard.The FA in the supplementary concentrate were extracted and methylated using the one-step procedure described by Sukhija & Palmquist (1988) and then analyzed under the same gas chromatography conditions as those described herein for meat FA.

Statistical analyses
Differences in FA were assessed by analysis of variance using the general linear model (GLM) of the SPSS for Windows 18.0 package (SPSS Inc., Chicago, IL, USA), including the fixed effects of production system and gender.The linear model used for each parameter was as follows: where Y ijk = observations for dependent variables; µ = overall mean; PS i = fixed effect of production system (i = organic system or conventional system); G j = fixed effect of gender; PS × G = interactions between production system and gender, and ε ijk = random effect of residual.
Gender has a low impact on goat kid meat quality.In meat from female goat kids, the proportions of C17:1, C18:3 n-3, (p < 0.05) and C18:1 trans-11  (p < 0.01) were greater and C18:0 was lower (p < 0.01) than in male goat kids.Meat from female goat kids had higher percentages of MUFA, UFA and CLA (p < 0.05) and lower SFA percentage (p < 0.05) than meat from males.Meat from conventionally reared female goat kids had higher CLA cis-9, trans-11 (RA) content than meat from conventionally reared males or organically reared males or females (p < 0.05).Regarding the fat depots, no differences between male and female kids were observed for the most studied parameters; there were only differences between groups for C18:2 n-6 cis, C18:2 n-6 trans and n-6 PUFA (p < 0.05) in the kidney fat, and for C16:1 n-9 (p < 0.05) in the pelvic fat.

Discussion
The FA ratio (C16:0, C18:0 and C18:1 n-9 cis) in the muscle tissue and fat depots of goat kids were in the range of those reported for unweaned ruminants (Mahgoub et al., 2002;Todaro et al., 2004;Santos et al., 2007;Nudda et al., 2008;Horcada et al., 2012) and weaned ruminants (Bas et al., 2005) and were also similar to those reported for other red-meat animal species (Banskalieva et al., 2000).Differences in FA composition between fat depots of farm animals have been demonstrated (Duncan & Garton, 1967).Generally, there is a progressive increase in saturation from peripheral to deep sites in farm animals (Wood, 1984;Casey & Van Niekerk, 1985;Potchoiba et al., 1990).
In the present study, the kids were fed exclusively with milk by suckling their dams, and even though the suckled milk is the main factor that influence the FA composition, since milk composition was not monitored, this will have to be tested in future studies.However, it seems opportune to discuss the feeding of the dams (the principal difference is the major consumption of concentrates per animal and year in the conventional farm, see M&M) and how it influences the milk composition.In fact, during the suckling phase, when goat kids are functionally non-ruminants, no ruminal biohydrogenation of the milk FA occurs prior to absorption by the intestine; thus, differences in the meat FA profile reflects the FA profile of the suckled milk (Sanz Sampelayo et al., 2006;Nudda et al., 2008).The C18:2 n-6, C18:3 n-3 and total PUFA ratios were similar to those reported in other goat studies (Banskalieva et al., 2000;Mahgoub et al., 2002;Todaro et al., 2004;Bas et al., 2005;Werdi Pratiwi et al., 2007).Nevertheless, these proportions were lower than those reported in other studies (Yeom et al., 2002;Nudda et al., 2008), likely due to the higher concentration of C18:2 n-6 and C18:3 n-3 FA in the supplemented feed to the dams.
In the present study, the CLA content in muscle and fat depots was similar or slightly higher than that reported by Todaro et al. (2004) in pelvic fat from suckling kids, but was lower than that reported for the intramuscular fat of suckling kids from lactating dams on diets supplemented with concentrates rich in C18:2 and C18:3 (Nudda et al., 2008) or in PUFA-rich pro-tected fat (Sanz Sampelayo et al., 2006).Also was lower than that reported in intramuscular fat depot by Horcada et al. (2012) in different Spanish breeds; however, the authors did not specify in detail the feeding management, especially with regard to food supplemented, which would be important to explain the differences found.Although grazing animals on grass pasture have higher CLA concentrations in their milk (Atti et al., 2006;Butler et al., 2008;D'Urso et al., 2008;Lucas et al., 2008;Pajor et al., 2009) and meat (Caputi et al., 2007;Paradis et al., 2008;Talpur et al., 2008), compared to non or low grazing animals; the feeding on Mediterranean shrublands or a diet containing tannins did not increase the milk (Tsiplakou et al., 2006;Mancilla-Leytón et al., 2013;Delgado-Pertíñez et al., 2013) or meat (Vasta et al., 2007) CLA contents.These results could be due to effects of tannins on ruminal biohydrogenation (Vasta et al., 2009(Vasta et al., , 2010) ) and although in present study goat kids were fed exclusively by suckling, this could explain the lack of effect showed on meat.High CLA concentrations can also be achieved by high-concentrate diets supplemented with whole oily seeds or their oils (Sanz Sampelayo et al., 2007;Nudda et al., 2008).Nudda et al. (2008) also observed strong relationships between the concentrations of VA, RA and linolenic acid in the muscle of suckling kids and those in their mothers' milk.This way, the higher intake of concentrate enriched by C18:2 and PUFA in the conventional lactating does, due to the ingredients of the concentrate (i.e.18% of soybean meal, see Table 1), could explain the higher CLA content in the conventional kids in the fat depots.Moreover, in the present study we have shown higher CLA desaturase index of the muscle of the kids from the conventional system than the kids from the organic system.However, the opposite happened for the fat depots.This might be explained because for kids suckling from goats fed on concentrate-rich diets, VA desaturation to CLA primarily occurs in the muscle rather than the mammary gland (Nudda et al., 2008), probably in response to an increase in desaturase gene expression induced by insulin (Daniel et al., 2004), and this could explain the greater value of CLA desaturase index in the muscle of the conventional kids.Nevertheless, lower desaturase activity associated with higher content of RA in milk fat (Morales et al., 2000) and in tissues (Palmquist et al., 2004) has been reported, and that might explain the lower desaturase activity in fat depots of the conventional kids.These differences between tissues suggest a different metabolic control of the fat deposition and needs to be determined in future studies.
The n-3 FAs are considered the most important dietary FA for human health.Current human health recommendations include a dietary n-6:n-3 FA optimum of 2.0-2.5, but most human foodstuffs have a ratio nearer to 5.0-10.0(MacRae et al., 2005).In the present study, the n-6 PUFA:n-3 PUFA ratio was lower than those reported in other studies on goats (Todaro et al., 2004;Sanz Sampelayo et al., 2006;Nudda et al., 2008) but was comparable to those reported for the fat depots and muscles of grazing goats (Bas et al., 2005;Horcada et al., 2012).In addition, organic kid meat and specially the fat depots displayed higher percentages of n-3 FAs than conventionally reared meat, which might be a consequence of high pasture intake by organically managed dams due to reduced feedstuff supplementation.In this regard, goats fed on rangeland (herbaceous plants, leaves and shrubs) (Bas et al., 2005) and sheep fed on grass pasture (Bas & Morand-Fehr, 2000) have shown to have higher n-3 FA ratios in fat and muscle than animals fed diets based on concentrate.Also, because of potentially increased risks of atherogenicity of C16:0, fat with a high atherogenicity index is assumed to be detrimental to human health (Ulbricht & Southgate, 1991).Except for pelvic fat, in this study there were no significant differences between the atherogenicity index in goat kid from organic or conventional managed dams.There are no known values of this index in studies of goats, nevertheless, the index values for both groups were lower that those reported in milk of sheep fed Mediterranean forages (Addis et al., 2005).The low fat content and FA profile (especially the PUFA content and the n-6:n-3 PUFA ratio) of meat from kids reared in both production systems indicates the beneficial characteristics of this meat with respect to human health.
Gender effects on the FA profile in meat are inconsistent (Banskalieva et al., 2000).No or minimal effects of gender on the FA profiles in meat (Nudda et al., 2008) or fat depots (Rojas et al., 1994;Mahgoub et al., 2002;Todaro et al., 2004) have been reported.In agreement with our results, Banskalieva et al. (2000) reported higher levels of C18:1 and lower levels of C18:0 in meat from females than males.Mahgoub et al. (2002) and Santos et al. (2007) reported that meat from males had higher levels of C15, C18:2 and C18:3 but lower levels of total C10, C14, C16, C18 and C18:1 than meat from females.The effects of sex on FA composition are reduce and may be explained in terms of differences in overall fat contents (Wood, 1984).The overall fat content of the animal and muscle have an important impact on proportionate fatty acid composition because of the different fatty acid compositions of neutral lipid and phospholipid (Wood et al., 2008).The major lipid class in adipose tissue (> 90%) is triacylglycerol or neutral lipid.In muscle, a significant proportion is phospholipid, which has a much higher PUFA content in order to perform its function as a constituent of cellular membranes (Wood et al., 2008).In the present study, minimal effects in fat depots have been obtained, in agreement with the results of Matsuoka et al. (1997) for Japanese Saanen goats which show that sex differences in fatty acid composition are more pronounced in phospholipids than in neutral lipids.
The results obtained in the present experiment indicates that the muscle and adipose tissues of suckling kids, coming from organic and conventional livestock production systems, are different only in some FA percentages.This fact could be due because the dams, in both experimental farms, were managed in a similar way based on the grazing of natural pastures.As consequence, conventional grazing-based management farms could be easily transformed into organic production livestock's.The effect of sex on FA profile was reduced.

Table 1 .
Fatty acid composition of muscle and fat depots of Payoya goat kids761 Proximate chemical composition and fatty acid profile of the concentrate supplements for conventional and organic livestock production systems

Table 2 .
Fatty acid profile (% of total fatty acids) in the Longissimus thoracis muscle of suckling Payoya kids according to livestock production system and gender unsaturated fatty acids; CLA, total conjugated linoleic acid, CLA cis-9, trans-11 + CLA trans-10, cis-12 + CLA cis-9, cis-11; n-3, all fatty acids with last double bond at 3 rd carbon from the methyl end; n-6, all fatty acids with the last double bond at 6 th carbon from the methyl end; Δ9C16, Δ9C16

Table 3 .
Fatty acid profile (% of total fatty acids) in the kidney adipose tissue of suckling Payoya kids according to livestock production system and gender

Table 4 .
Fatty acid composition of muscle and fat depots of Payoya goat kids765 Fatty acid profile (% of total fatty acids) in the pelvic adipose tissue of suckling Payoya kids according to livestock production system and gender