Improvement of fatty acid profiles in kid meat from Murciano-Granadina goats under semi-arid environment

Abstract

The present paper shows the results of a comparison of the fatty acid profile of kid meat obtained from extensive management system under semi-arid conditions and conventional systems. Meat samples from 61 Murciano-Granadina goat kids reared in extensive management system (9 females, 12 males) under semi-arid conditions and two variants of conventional managing systems, intensive with natural rearing (9 females, 11 males) and intensive with artificial rearing (10 females, 10 males), were used in the present study. Kids reared under the extensive management system showed (P < 0.05) that their intramuscular fat depots had the lowest percentage of myristic acid (12.31%) and the highest percentage of oleic acid (36.66%). A strong influence of physical activity during grazing in pasture modulated the fatty acid profile in muscle of kids reared under the extensive management system. Kids from this management system show a trend to produce healthier meat relative to intensive with natural and with artificial rearing management systems, as reflected by the fact that the lowest atherogenicity index was measured in intramuscular fat from kids reared under extensive management system.

Keywords:

• extensive system
• atherogenicity index
• grazing

1. Introduction

In the semi-arid regions of southeastern Spain, where grazing has a long history which date to the Bronze Age, grazing has become fundamental to the maintenance of vegetal species diversity. Although goat meat is very poorly valued (Dubeuf et al. 2004) in Europe, in some European countries with semi-arid regions such as Spain, Italy, Portugal or Greece the goat meat is very much appreciated and is a profitable and important part of the income of breeders (Working Group FAO/CIHEAM 2002). Traditional production systems using the semi-arid resources are becoming marginalized, and goat productivity is very low as a result of the long and pronounced dry season which often causes serious food shortages for the livestock, leading to diseases and increased mortality.

Although it is known that moderate grazing has a positive effect on plant fitness, domestic goat production has also been considered to be extremely detrimental to vegetation, due to the impact on soils and direct damage to plants (Dhillion et al. 2004). Due to the fact that in areas where the grazing activity has been kept and these negative effects have not appeared, we must find some way to increase the profits of the goat grazing activity in these areas. Although few studies have been developed in order to show if goat meat from extensive management system is healthier or has higher quality than goat meat from intensive with natural rearing management system and intensive with artificial rearing management system, Zurita-Herrera et al. (2011) characterized the goat meat quality from intensive with artificial rearing management system, intensive with natural rearing management system and extensive management system using canonical discriminant analysis and clustering, and found that the intensive with artificial rearing management system seemed to affect meat quality negatively in contrast with the meat obtained from the extensive management system, which had the best meat quality, and the intensive with natural rearing management system.

Goat meat production in semi-arid regions under good management strategies could produce healthier meat as well as preserves the semi-arid region if appropriated management strategies in order to reduce vegetation degradation are applied. The present study assesses the fatty acid profile of the extensive kid meat, dealing with differences in the fatty acid composition (particularly with regard to long-chain fatty acids) of the extensive meat with respect to conventional management systems (intensive with artificial rearing and intensive with natural rearing) in order to prove if goat meat production from extensive systems is healthier than from conventional systems.

2. Material and methods

2.1. Animals and management systems

Sixty-one Murciano-Granadina kids (28 females, 33 males) from the herd located in the experimental farm of Diputación de Granada (Granada, Spain) were raised under three different management systems (extensive, intensive with natural rearing and intensive with artificial rearing) from birth to their slaughtering at around 34–38 days old, and they reached 7 ± 1 kg of live weight. The feeding period started in January. The 21 kids (9 females, 12 males) in the extensive management system (hereafter “E”) suckled directly from dams and were raised on a free-range pasture containing mostly wheat (Triticum Sativum Lam. T. Vulgare), oat (Avena sativa) and chickpeas (Cicer arietinum), with no additional supplement. This management system was situated in the village of Pedro Martínez (37°51′ latitude, −3°22′ longitude and 1042 m.a.s.l.), located in the West Mounts (Granada, South East of Spain), where the climate is Mediterranean semi-arid, with an average annual rainfall of 300 mm. Kids (9 females, 11 males) in the intensive with natural rearing management system (hereafter “IN”) suckled directly from dams and had access to alfalfa hay and cereal straw. The IN kids and the dams did not have access to pasture. The 20 kids (10 females, 10 males) in the intensive with artificial rearing management system (hereafter “IA”) were separated from dams after birth, housed in a nursing parlour and fed colostrum for the first 2 days, as described by Castro et al. (2005). Then, kids had free access to milk replacer 24 h a day (Univet lambs and kids 60, Nutral S.A., Madrid, Spain; ash, 6.00%; cellulose, 0.04%; protein, 24.00%; and fat, 24.50% on dry matter) that was distributed by a nursing device. This feeding regimen was supplemented with alfalfa hay and cereal straw. Kids from all the three systems had free access to water at all times.

2.2. Slaughtering procedure

Animals were slaughtered according to the guidelines of the Council Directive 86/609/EEC (European Communities 1986). They were slaughtered at Los Filabres S.C.A. when their body live weight reached 7 ± 1 kg. Kids were fasted with free access to water during the 24 h before slaughter and were slaughtered using captive bolt stunning followed by throat cut to sever carotid arteries and jugular veins.

Kids were dressed according to Colomer-Rocher et al. (1987). Hot (after slaughter) and chilled (after 24 h chilling at 4°C) carcass weight (PCE-HS 50, maximum = 50 kg, e = 20 g, PCE Group Ibérica, Albacete, Spain) and weights of the head, skin, heart, liver, lungs and trachea, kidney, full and empty gastrointestinal tract (gastrointestinal content was determined as the difference between them) and spleen were recorded using electronic weights (G-310, maximum = 15 kg, e = 5 g, Dibal S.A., Bilbao, Spain; and Tefal model Gourmet, maximum = 5 kg, e = 1 g, Groupe SEB Ibérica, Barcelona, Spain).

After chilling (24 h at 4°C), carcasses were split. The left side was divided into five primal cuts (neck, flank, ribs, shoulder and long leg) and three minor cuts (kidney, kidney fat and tail) as described by Colomer-Rocher et al. (1987). Primal cuts were weighed (Tefal model Gourmet) and dissected into separable tissues (subcutaneous and intermuscular fat, lean and bone). The separable tissues were weighed as described above, and fat samples were frozen (−20°C) until analysis.

2.3. Fatty acid composition

Fatty acid from triceps brachii muscle and intermuscular and subcutaneous fat samples obtained from the shoulder were extracted as described by Folch et al. (1957). Briefly, fatty acids were separated before derivatization (ISO Norm 5509, 2000) in a gas chromatograph (Model HP 5890 Series II GC; Hewlett–Packard, Avondale, PA) equipped with a flame ionization detector and a phenyl-methyl-siloxane (cross-linked at 5%) capillary column (30 m long, 0.25 mm internal diameter, film thickness of 0.25 µm). The detector and the injector were maintained at 280°C. The carrier gas was helium at a flow rate of 1 ml/min and a division ratio of 100:1.

The atherogenicity index was calculated using the equation developed by Ulbricht and Southgate (1991):

where MUFA is monounsaturated fatty acids and PUFA is polyunsaturated fatty acids.

2.4. Statistical analyses

A two-way ANOVA model (SAS Institute Inc. 1999–2001, v. 8.2 for Windows, Cary, North Carolina, USA) including the fixed effects of the management system and sex was performed that described the interaction between them. A Duncan post hoc test of mean homogeneity (SAS Institute Inc. 1999–2001, v. 8.2 for Windows, Cary, North Carolina, USA) was developed to test the individual separation of means. Threshold level of probability to declare the statistical significance of the difference between pairs of means was P < 0.05.

3. Results and discussion

The fatty acid percentages in intramuscular (triceps brachii muscle), subcutaneous and intermuscular fat deposits are shown in Tables 1, 2 and 3, respectively. The saturated fatty acid (SFA) percentages ranged from 45.23% to 63.91%, which is consistent with those reported by Bañón et al. (2006) and García-Navarro et al. (2008) but higher than those reported by Peña et al. (2009). SFA percentage is studied because it increases the concentration of blood cholesterol, although the different SFAs have different effects on cholesterol concentration. For example, lauric (C12:0), myristic (C14:0) and palmitic (C16:0) acids raise the plasma cholesterol level (Denke & Grundy 1992), whereas stearic acid (C18:0) does not appear to have such an effect and is considered ‘neutral’ (Ascherio 2003). While is clear that C14:0 and C16:0 are responsible for increasing the total plasma cholesterol concentration and the low density lipoprotein (LDL) cholesterol concentration, the other major SFA, C18:0 is not hypercholesterolaemic and does not increase the total plasma cholesterol concentration or LDL cholesterol concentration (Ascherio 2003). In addition, C18:0 is partially converted to oleic acid in vivo and has not been shown to elevate blood cholesterol (Valsta et al. 2005). High dietary intake of long-chain SFA, except stearic acid, has been associated with increase in plasma cholesterol levels and hence pose a higher risk for atherosclerosis (Ascherio 2003).

Table 1. Effect of management system and sex on fatty acid composition (% total of fatty acids) of triceps brachii muscle.

	Management system			Sex
Fatty acid composition, %	E	IN	IA	Male	Female	SEM
C6:0	0.01	0.15	0.02	0.01	0.12	0.05
C11:0	nd	nd	0.02	0.01	nd	0.00
C12:0	0.36	0.83	1.67	1.12	0.55	0.30
C13:0	5.52	3.92	4.74	5.00	4.46	0.42
C14:0	12.31^b	19.27^a	21.29^a	17.53	16.48	1.37
C14:1	0.03	0.01	0.61	0.27	0.05	0.12
C15:0	0.29^ab	0.06^b	0.63^a	0.21	0.39	0.08
C15:1	0.06^a	nd	0.17^b	0.05	0.09	0.02
C16:0	25.31^a	23.02^ab	21.27^b	24.01	22.82	0.64
C16:1	0.43	0.27	0.63	0.31	0.56	0.09
C16:2	1.09	0.99	0.60	0.95	0.91	0.11
C16:3	0.36^b	0.09^a	0.23^ab	0.21	0.26	0.03
C16:4	0.06	nd	0.10	0.03	0.08	0.01
C17:1	0.14^a	0.02^a	1.38^b	0.04	0.87	0.22
C18:0	12.81	13.26	11.51	12.34	13.00	0.51
C18:1	36.66^b	29.85^a	28.35^a	32.87	31.25	1.24
C18:2	1.61^b	4.93^a	2.29^b	3.13	2.67	0.63
C18:3	0.10^ab	0.01^a	0.27^b	0.07	0.16	0.03
C18:4	0.03	0.02	0.05	0.01	0.06	0.01
C20:0	0.23	0.05	0.09	0.17	0.08	0.05
C20:1	0.04	0.04	0.1	0.02	0.09	0.01
C20:3	nd	nd	0.01	0.00	nd	0.00
C20:4	0.57	0.79	0.83	0.50	0.98	0.20
C20:5	0.03	nd	0.12	0.04	0.04	0.02
C22:0	0.01	0.07	0.00	0.03	0.03	0.01
C22:2	0.18	0.24	0.30	0.16	0.32	0.06
C23:0	0.73	1.15	0.21	0.42	1.15	0.23
C24:0	0.01^b	0.38^a	0.12^ab	0.13	0.22	0.05
C24:4	0.10	nd	0.00	0.07	nd	0.03
C26:6	0.00	nd	0.05	0.03	nd	0.01
All SFA	58.52	63.01	63.91	61.34	61.63	1.11
All MUFA	37.36^b	30.19^a	31.23^a	33.57	32.90	1.13
All PUFA	4.12	6.81	4.86	5.08	5.47	0.73
AI	1.81^b	2.73^a	3.00^a	2.46	2.32	0.25

Note: Means with different superscript letters differ significantly (P < 0.05).

SEM, standard error of the mean; nd, not detected.

Atherogenicity index (AI) = (C12:0 + (4 × C14:0) + C16:0)/(MUFA + PUFA) (Ulbricht & Southgate 1991).

Table 2. Effect of management system and sex on the fatty acid composition (% total of fatty acids) of subcutaneous shoulder fat.

	Management system			Sex
Fatty acid composition, %	E	IN	IA	Male	Female	SEM
C6:0	0.00	0.00	0.04	0.00	0.03	0.01
C8:0	0.27	0.08	0.07	0.16	0.11	0.07
C10:0	0.16	0.27	0.24	0.12	0.32	0.07
C11:0	0.00	0.00	0.07	0.00	0.05	0.02
C12:0	0.61	1.59	1.40	1.15	1.23	0.36
C13:0	1.26	1.44	0.71	1.43	0.80	0.16
C14:0	8.98	9.51	8.65	9.23	8.78	0.51
C14:1	0.15	0.06	0.17	0.09	0.17	0.02
C15:0	0.69	0.07	0.61	0.57	0.43	0.12
C15:1	0.17^ab	0.01^a	0.28^b	0.12	0.22	0.04
C16:0	28.27	29.37	28.75	29.14	28.42	0.83
C16:1	1.00	0.66	1.07	1.05	0.84	0.16
C16:2	0.95	0.65	0.76	0.61	0.96	0.16
C16:3	0.62^b	0.14^a	0.46^b	0.40	0.45	0.05
C16:4	0.22^b	0.02^a	0.03^a	0.10	0.08	0.03
C17:1	0.12^a	0.03^a	0.37^b	0.11	0.27	0.05
C18:0	14.66^b	9.22^a	14.05^b	12.67	13.22	0.64
C18:1	40.43	44.77	40.81	41.36	42.08	0.96
C18:2	1.36	2.09	1.05	1.37	1.49	0.19
C18:3	0.00	nd	0.02	nd	0.01	0.01
C18:4	nd	0.00	0.07	0.04	0.02	0.01
C20:1	0.01	0.02	0.01	0.01	0.02	0.01
C22:2	0.01	nd	0.29	0.25	0.01	0.10
C23:0	0.03	0.00	0.00	0.02	0.01	0.01
C24:0	0.01	0.00	0.00	0.00	0.00	0.00
All SFA	54.94	51.55	54.58	54.48	53.38	0.98
All MUFA	41.89	45.55	42.72	42.75	43.59	0.94
All PUFA	3.17	2.90	2.69	2.77	3.02	0.17
AI	1.44	1.42	1.43	1.48	1.39	0.21

Note: Means with different superscript letters differ significantly (P < 0.05)

SEM, standard error of the mean; nd, not detected.

Atherogenicity index (AI) = (C12:0 + (4 × C14:0) + C16:0)/(MUFA + PUFA) (Ulbricht & Southgate 1991).

Table 3. Effect of management system and sex on fatty acid composition (% total of fatty acids) of intermuscular shoulder fat.

	Management system			Sex
Fatty acid composition, %	E	IN	IA	Male	Female	SEM
C8:0	N.D	0.14	0.11	0.06	0.09	0.05
C10:0	0.08	0.20	0.20	0.12	0.19	0.06
C12:0	0.14^b	1.43^a	0.50^ab	0.60	0.55	0.19
C13:0	0.35^b	1.99^a	1.06^ab	0.81	1.18	0.23
C14:0	5.55	5.72	6.65	4.77	7.17	0.89
C14:1	4.33	4.28	4.02	4.80	3.65	1.08
C15:0	0.29	0.20	0.92	0.15	0.88	0.22
C15:1	0.07	1.88	0.16	0.04	0.89	0.39
C16:0	33.44	30.11	31.29	31.66	31.93	1.15
C16:1	0.76	0.97	1.05	0.78	1.06	0.18
C16:2	0.73	0.42	0.88	0.68	0.77	0.16
C16:3	0.32	0.16	0.42	0.17	0.47	0.06
C16:4	nd	nd	0.01	nd	0.01	0.00
C17:1	0.17	0.06	0.17	0.11	0.18	0.04
C18:0	10.78^b	5.33^a	10.41^b	8.98	9.87	0.97
C18:1	41.93	44.48	41.00	43.36	38.36	0.99
C18:2	0.61^b	2.44^a	0.70^b	0.83	1.24	0.25
C18:3	nd	0.01	0.04	0.02	0.02	0.00
C18:4	nd	0.03	0.03	0.00	0.04	0.01
C20:0	nd	0.08	0.14	0.12	0.04	0.03
C20:1	nd	0.02	0.05	0.04	0.01	0.01
C20:4	nd	0.00	0.01	0.01	0.00	0.00
C22:2	0.01	0.02	0.13	0.04	0.08	0.03
C23:0	nd	0.01	0.01	0.01	0.01	0.01
C26:6	nd	0.00	0.01	0.00	0.00	0.00
All SFA	52.60	45.23	51.32	47.28	53.24	1.71
All MUFA	45.73	51.69	46.46	51.00	44.13	1.80
All PUFA	1.67	3.08	2.22	1.72	2.63	0.29
AI	1.17	0.99	1.19	0.97	1.30	0.23

Note: Means with different superscript letters differ significantly (P < 0.05).

SEM, standard error of the mean; nd, not detected.

Atherogenicity index (AI) = (C12:0 + (4 × C14:0) + C16:0)/(MUFA + PUFA) (Ulbricht & Southgate 1991).

Management system did affect significantly (P < 0.05) the SFA percentages in triceps brachii muscle, subcutaneous and intermuscular shoulder fat. In the triceps brachii muscle, the main SFA identified were myristic, palmitic and stearic acids, with percentages in the range of 12.31–21.29%, 21.27–25.31% and 11.51–13.26%, respectively, which were in the range of those reported in goats (Bas et al. 2005; Peña et al. 2009; Horcada et al. 2010, 2012), and were in agreement with the studies by Beserra et al. (2004), among other authors. Myristic acid percentage was higher in our study. Santos et al. (2007) found higher palmitic and stearic acid percentages in kids from Serrana, Bravia and Serrana × Bravia cross-bred genotypes slaughtered at 8–11 kg, and Atti et al. (2013) found higher stearic percentages in lambs slaughter at 28–30 kg. These differences are probably due to the different weight at slaughter.

The E samples had the lowest C14:0 percentages and the highest C16:0 percentages, and IN and IA showed similar percentages (P < 0.05). In subcutaneous and intermuscular shoulder fat, the lowest C18:0 percentages (P < 0.05) were found in the IN samples, and those values were in agreement with a previous report (García-Navarro et al. 2008), but in the intermuscular shoulder fat samples, the highest C12:0 and C13:0 percentages (P < 0.05) were found in the IN samples. The C14:0 intramuscular percentage (P < 0.05) was the lowest in extensive meat. In rabbits, Hougham and Cramer (1980) demonstrated that although average percentages of C14:0 in triceps brachii muscle were lower (P < 0.05) than in sheep and beef (Banskalieva et al. 2000), the average percentages (P < 0.05) of C16:0 and C18:0 in the same muscle were similar in animals with high-activity metabolic profiles which have larger amounts of 18-carbon fatty acids at the expense of 14- and 16-carbon fatty acids. This argument may explain the lower myristic fatty acid intramuscular percentage observed in extensive animals. In the current study, the intramuscular palmitic fatty acid percentage was not the lowest in E animals, but 18-carbon fatty acids (mainly oleic acid) were elevated at the expense of myristic fatty acid.

Sex did not affect the SFA percentages in any fat deposit, but it must be said that sex differences in fatty acid composition in the literature have been inconsistent. Banskalieva et al. (2000) reported that female goats had lower levels of C14:0 and C18:0.

The MUFA percentages were mainly due to oleic acid (C18:1), which lowers lipaemia by reducing both the cholesterol raising LDL and the triglycerides (Rao et al. 2003).

The C18:1 concentration (mainly determining total MUFA) in goats is similar to that in other species, but the mean concentration of C16:1 in goat muscles is higher compared with lambs (Banskalieva et al. 2000). The oleic acid had the highest percentage compared to other fatty acids, although the values recorded in this study were those reported by Marichal et al. (2003) for Canary Caprine Groups kid goats slaughtered at 6 kg and 10 kg, by Peña et al. (2009) for Criollo Cordobes and Anglo-Nubian kids produced under extensive feeding conditions and slaughtered at 11 kg, and lower than those obtained from weaned goats by Bas et al. (2005) and Talpur et al. (2008).

The type of management system did not affect the percentage of C18:1 in subcutaneous or intermuscular deposits. In contrast, this percentage was greater (P < 0.05) in the triceps brachii muscle samples from the E carcasses. As reported previously, the relatively high muscular activity of E animals causes a reduction in C14:0 content with a concomitant rise in the abundance of 18-carbon fatty acids (Hougham and Cramer 1980). Angood et al. (2008) did not observe that any management system affects the relative abundance of C18:1 in lambs. The lambs in that study were older than the kids in our current study, which may explain the contrasting results observed in the two studies. It has been reported that increasing age of slaughter of weaned kids receiving a concentrate-based diet decreases the MUFA level in kidney and subcutaneous adipose tissues (Bas et al. 1987). Bas et al. (1982) pointed out that level of branched-chain fatty acids (saturated C14, C15 and C16) in subcutaneous fat was higher in intact than castrated kids. Sex had not an effect on MUFA percentages.

As it was reported by Banskalieva et al. (2000), PUFA percentages were mainly due to linoleic (C18:2), linolenic (C18:3) and arachidonic (C20:4) fatty acids. The percentage of C18:2 in intermuscular and intramuscular deposits in IN and IA carcasses was significantly greater (P < 0.05) than in extensive meat. A similar trend was observed in subcutaneous deposits, although the difference was not statistically significant. The feedstuff for the IN dams was prepared with sunflower meal, and Eknaes et al. (2009) recently demonstrated that inclusion of sunflower in goat feed increases the C18:2 in milk. This increase may have resulted in the observed increase in this acid in IN fat deposits. In addition, the diet for E dams did not include any sunflower, and the percentage of C18:2 in intensive milk replacer was very low (approximately 3%, data provided by manufacturer). It is well established that docosahexaenoic acid (DHA) and eicosapentaenoic acid (EPA) are beneficial to human health (Horrocks and Yeo 1999), but meat and meat products generally do not contain substantial levels of these fatty acids. Fortunately, goat meat from the IA showed high levels of EPA (C20:5). The highest concentration of long-chain n–3 PUFA was found in the triceps brachii samples from the IA, and in fact, the consumption of goat meat from IA with increased n–3 fatty acid concentration can contribute to human requirements for these fatty acids, especially alpha linolenic acid (C18:3n–3), EPA, docosapentaenoic acid and DHA. Meat, milk and eggs are the only sources of long-chain n–3 PUFA in the diet of people who do not consume fish. Long-chain n–3 PUFA like EPA and DHA play an important role in the development of cerebral and retinal tissues and in the prevention of heart diseases and some cancers (Simopoulos 2002). In addition, a high proportion of linolenic acid is beneficial for human health due to their capacity to diminish thrombotic tendency in blood and the risk of suffering coronary diseases (Cañeque et al. 2003; Webb et al. 2005).

The results reported in Tables 1, 2 and 3 support the notion that EPA is indeed present in goat kid meat, suggesting that consumption of this meat may have health benefits in a general sense.

The atherogenicity index (Ulbricht & Southgate 1991) values in subcutaneous and intermuscular fat deposits were not affected by the type of management system. In contrast, the muscle fat deposit was affected by the type of management system, with E samples showing the lowest atherogenicity index (1.81; P < 0.05). The reason for these differences is probably the low C14:0 percentage and high C18:0 percentage in the E muscle fat deposit because both percentages are modulated by grazing-related muscular activity. Fehily et al. (1994) reported that an increase of 0.2 in the atherogenicity index is associated with an increase in plasma cholesterol of 1.93 mg/dL. Although further should be performed, the consumption of E kid meat may have greater health benefits compared with consumption of conventional kid meat. The sex did not affect the atherogenicity index of any fat deposit.

4. Conclusions

Fatty acid composition is influenced by the management systems, being the meat from the extensive system under semi-arid conditions the one with the highest oleic fatty acid content and lowest SFA content, as well as the lowest atherogenicity index. Although further studies are required, our results suggest that meat from extensive system is truly unique and could provide more health benefits than meat from conventional systems. This could help to maintain the grazing activity in semi-arid regions and prevent these areas from abandonment.

Acknowledgements

The authors thank Diputación de Granada, Murciano-Granadina National Breeders Association and Andalusian Co-operative Society Los Filabres for their financial support for this study.