Results and discussion
The total lipid content of ruminant tissues is comprised of about 40 %
SFA, 40 % MUFA (monounsaturated fatty acids) and 2–25 % PUFA (Wood et
al., 2008). Although ruminant meat is an important source of nutrients, its
relatively high content of SFA has been criticized and linked with an
increase in total cholesterol; consequently, it has been related to cardiovascular
diseases (Ribeiro et al., 2011). Nevertheless, it has been evidenced that
individual fatty acids in this family have considerably different effects.
For instance, lauric acid (C12:0) and myristic acid (C14:0) have a greater
total cholesterol raising effect than palmitic acid (C16:0), whereas stearic
acid (C18:0) has a neutral effect on the concentration of total serum
cholesterol, including no apparent impact on either low-density lipoprotein
or high-density lipoprotein (Daley et al., 2010). Within the SFA, the
predominant ones in ruminant meat are palmitic (C16:0), stearic (C18:0) and
myristic (C14:0) fatty acids (Cruz et al., 2011). Forest plots illustrating
C16:0, C18:0 and C14:0 of Mediterranean lambs are presented in Fig. 1a, b
and c, respectively.
Data used for a meta-analysis of myristic acid (C14:0) were compiled from
five studies and altogether included 82 lambs. Lambs of the Merino Branco, Churra
Tensina,a,b the Talaverana and Pramenka
breeds were used for the analysis. The overall pooled result for C14:0 was
5.32 %, with a 95 % CI of 4.81–5.82 %. All studies included in
the analysis were within the range of the overall estimate.
The meta-analysis of palmitic acid (C16:0) was compiled from five individual
studies and altogether included 82 lambs of the Merino Branco, Churra
Tensinaa,b, Talaverana and Pramenka breeds. The overall pooled result
(estimate) for C16:0 was 22.85 %, with a 95 % confidence interval (CI)
from 20.71 to 24.99. This result gave us an estimate of the mean effect size
and its precision. The study that included Talaverana lambs was not within the
range of the overall pooled result. Talaverana lambs had 26.39 % of C16:0, with a 95 % confidence interval from 25.96 to 26.82. This result could be
due to the fact that Talaverana lambs were weaned, while all other breeds
included in meta-analysis were suckled by their dams until slaughter. According to
Bas and Morand-Fehr (2000), this effect could be due to the presence of some fatty
acids laid down in adipose tissue before weaning , de novo endogenous synthesis of
fatty acids, the length of the post-weaning period, the fattening level, and the age and
weight at weaning.
Stearic (C18:0) fatty acid was analysed using a data from six studies.
Altogether, it included 92 lambs of the Merino Branco, Comisana, Churra
Tensinaa,b, Talaverana and Pramenka breeds. The overall pooled result
for C18:0 was 14.78 %, with a 95 % CI from 13.66 to 15.89. All studies
included in the analysis were within the range of the overall estimate.
Although not significantly different, the proportion of C18:0 in Talaverana
lambs (16.42) was slightly higher than in the other breeds included in the
study. Compared to the Talaverana lambs, which were weaned and had
a short starter diet at pasture, the feeding management of all other breeds included in the
study was based only on suckling and grazing. This feeding management of
Talaverana lambs could be followed by higher rumen biohydrogenation of
dietary PUFA, and therefore we assumed that they would have a significantly
higher proportion of C18:0 as linoleic (LA, C18:2) and α-linolenic acid (ALA, C18:3) are usually available in grains and forages.
They are extensively biohydrogenated in the rumen, resulting in a higher
outflow of C18:0 to the duodenum than the actual intake of C18:0 as well
fatty acids intermediates of biohydrogenation (trans-11 C18:1 vaccenic acid and
cis-9, trans-11 conjugated linoleic acid). The proportion of C18:0 in lambs of the Comisana
breed (16.23) was also close to Talaverana (16.42) but with a lower
weight of the study (15.43 vs. 17.27) and a larger 95 % CI (95 % CI
from 15.11 to 17.35 in Comisana vs. 95 % CI from 15.79 to 17.04 in
Talaverana). With smaller CI and higher weight assigned to the more
precise studies, it should be mentioned that the data of Talaverana lambs in our
analysis were more precise. The neutral effect of C18:0 on the concentration of
total serum cholesterol implies that this SFA may not increase the risk of cardiovascular disease (Daley et al., 2010). Therefore, a slightly higher
proportion of C18:0 in Talaverana lambs could be denoted as the most
desirable among the breeds included in our study. Nevertheless, the proportion of all other fatty acids and their
influence on a human health must be taken into consideration.
Beside the criteria included in these analyses, it must be considered that
C16:0, C18:0 and C14:0 are strongly associated with the overall fat levels in
breeds. This trait was not analysed in the present study because data for
overall fat levels of all included breeds were not available.
The analysis of SFA was performed using data from five individual studies and
included 84 lambs. The breeds included in the analysis were Comisana, Churra
Tensinaa,b, Talaverana and Pramenka. The overall pooled result of SFA
was 47.85, while a 95 % CI ranged from 44.16 to 51.55. All included studies
were within the range of the overall estimate (Fig. 1d). Although not
significantly different, proportions of SFA in Churra Tensinaa lambs
were slightly lower than the others. Taking into account that a lower
proportion of SFA is desirable from the perspective of the human health
(Prates and Bessa, 2009), the SFA proportion of the Churra Tensinaa
lambs can be considered as the most desirable among the breeds included in
this study.
Meta-analysis of C18:1 (a), C18:2 n-6 (b), C18:3 n-3 (c) and MUFA (d).
Different superscript letters (a,b) indicate lambs of the
same breed included in different studies; ES: effect size; CI: confidence
interval; RW: relative weight of the study; Overall: overall pooled result.
In contrast to SFA, it has been proven that MUFA and PUFA are beneficial for
human health (Prates and Bessa, 2009; Hoenselaar, 2012). The beneficial
effects of PUFA have been associated with its ability to protect against
cardiovascular diseases (Harris et al., 2007), whereas MUFAs have been
associated with a hypocholesterolemic effect and with a beneficial effect on
insulin sensitivity (Ros, 2003; López-Huertas, 2010). Approximately
50 % of the intramuscular fat of the lamb is made up of unsaturated fatty
acids; MUFAs are made up predominantly from oleic acid (C18:1) and PUFAs
from linoleic (LA, C18:2) and α-linolenic (ALA, C18:3) fatty acids,
respectively (McAfee et al., 2010). Oleic acid (C18:1) originates either
from dietary sources or endogenous synthesis of C18:0 by the enzyme complex
Δ9-desaturase (stearoyl-CoA desaturase). It has been considered to be
hypolipidemic, reducing plasma cholesterol as well as triglycerides (Mills
et al., 1992), and can be considered as a desirable component of the human
diet. A forest plot illustrating C18:1 of Mediterranean lambs is presented in
Fig. 2a. A meta-analysis was performed using data from six studies and
included the Comisana, Merino Branco, Talaverana, Churra Tensinaa,b and
Pramenka breeds. Altogether, 92 lambs were included in the analysis. The
overall pooled result for C18:1 was 32.53 %, with a 95 % CI from 29.96 to
35.11. Studies that included Churra Tensinaa,b lambs and Comisana lambs
were not within the range of the overall pooled result. Churra Tensinaa
lambs had 36.64 % of C18:1, with a 95 % confidence interval from 35.16 to
38.11, while Churra Tensinab lambs had 37.7 % of C18:1, with a 95 %
confidence interval from 36.67 to 38.72. By contrast, Comisana lambs
had 26.7 % of C18:1, with a 95 % confidence interval from 24.82 to 28.58.
According to Dervishi et al. (2010), the lipid profile of ruminants can be
manipulated by diet, and grazed lambs have a lower proportion of C18:1
compared to all other feeding systems. Because of this and the feeding
management of Churra Tensina and Comisana lambs, which were similar to other
breeds included in the study (based on suckling and grazing), we expected
that their proportions of C18:1 would be in the range of our overall
estimate. Nevertheless, it must be considered that C18:1 can also originate
from endogenous synthesis of C18:0 and could also be a major factor that had
an impact on our results. Mills et al. (1992) and Wood et al. (2003)
reported that diets with a higher proportion of C18:1 are regarded as
beneficial to human health. In accordance with this, Churra Tensinaa,b lambs
had significantly higher and consequently more favourable proportions of
C18:1 than the other breeds included in our study.
Meta-analysis of PUFA (a), PUFA / SFA ratio (b) and n-6 / n-3
ratio (c). Different superscript letters (a,b) indicate lambs of the
same breed included in different studies; ES: effect size; CI: confidence
interval; RW: relative weight of the study; Overall: overall pooled result.
Linoleic (LA; C18:2 n-6) and α-linolenic (ALA; C18:3 n-3) acids are
essential n-6 and n-3 PUFAs in humans, i.e. they are not synthesized by the
human body and should be taken up through the diet. They are precursors of potent
lipid mediators, termed eicosanoids, which have an important role in the
regulation of inflammation. Eicosanoids derived from n-6 PUFAs such as
arachidonic acid (C20:4 n-6) have proinflammatory and immunoactive
functions, whereas eicosanoids derived from n-3 PUFAs such as
eicosapentaenoic acid (C20:5 n-3) and docosahexaenoic acid (C22:6 n-3) have
anti-inflammatory properties, attributed to their ability to inhibit the
formation of n-6-PUFA-derived eicosanoids (Wall et al., 2010). However, it
must be considered that in ruminants, LA and ALA are degraded to MUFA and
SFA in the rumen by microbial biohydrogenation (70–95 and 85–100 %,
respectively) and only a small proportion, around 10 % of dietary
consumption, is available for incorporation into tissue lipids (Nieto and
Ros, 2012). A forest plot illustrating the LA of Mediterranean lambs is
presented in Fig. 2b. The analysis of LA was performed using a data from five studies. The analysis altogether included 82 lambs of the Merino Branco, Churra
Tensinaa,b, Talaverana and Pramenka breeds. The overall pooled result
was 5.60 %, with a 95 % CI from 3.67 to 7.54. The analysis showed that
the proportion of LA in Pramenka lambs was significantly lower (2.79 % of LA, with a 95 % confidence interval from 2.34 to 3.24) than the
overall pooled result and therefore than in the other breeds included in our
study. The
main dietary sources of LA (such as sunflower, safflower or corn oils) that
could influence its proportion in lamb meat were excluded from the
analysis (except for a short starter diet in Talaverana lambs). Thus, it was
expected that their proportions would be similar within the overall
pooled estimate.
A forest plot illustrating the α-linolenic (ALA, C18:3 n-3) acid of
Mediterranean lambs is presented in Fig. 2c. A meta-analysis of ALA was
compiled from four individual studies and altogether included 63 lambs of
the Merino Branco, Churra Tensinaa, Talaverana and Pramenka breeds. The
overall pooled result for ALA was 1.95 %, with a 95 % CI from 1.67 to
2.22. All studies included in the analysis were within the range of the
overall estimate. The main feeding and rearing systems (herbage and milk of
pasture-fed ewes) related to a higher content of ALA and its proportion in
lamb meat were included in the analysis (except for a short starter diet in
Talaverana lambs). Therefore, non-significant differences between lambs
included in our survey may be a consequence of similarity in feeding and
rearing systems.
Meta-analyses of MUFA and PUFA were compiled from five individual studies and
altogether included 84 lambs of Comisana, Churra Tensinaa,b, Talaverana
and Pramenka breeds. The overall pooled result for MUFA was 37.87 %, with a 95 % CI from 35.90 to 39.83. In this case all studies were within the
range of the overall estimate (Fig. 2d). The overall pooled result for
PUFA was 11.50 %, with a 95 % CI from 9.98 to 13.01. All studies were
within the range of the overall estimate (Fig. 3a). According to these
results it can be reported that the proportions of MUFA and PUFA between
the meat of the lambs included are very similar. Since it has been proven that
MUFA and PUFA are beneficial to human health (Prates and Bessa, 2009;
Hoenselaar, 2012), their proportions will have a similar beneficial impact on human health.
Nutritional value of meat is determined by the PUFA / SFA ratio and the
balance between fatty acids of the n-6 and n-3 series (Warren et al., 2008).
From a human health viewpoint the recommended values of the PUFA / SFA ratio
are higher than 0.45 (World Health Organization, 2003). Nevertheless, it
must be considered that meat from ruminants has a lower PUFA / SFA ratio than
that of non-ruminants because of the hydrogenating action of the rumen
microorganisms. In the present study, the analysis of PUFA / SFA ratio was
compiled from five studies and included 84 lambs of the Comisana, Churra
Tensinaa,b, Talaverana and Pramenka breeds. The overall pooled result
for the PUFA / SFA ratio was 0.23, with a 95 % CI from 0.21 to 0.25. All studies
were within the range of the overall estimate (Fig. 3b). The proportions
of the PUFA / SFA ratio between the meat of the lambs included are low but very similar.
Diets with a lower PUFA / SFA ratio of 0.45 are less healthy (Warren et al.,
2008) and therefore lower PUFA / SFA ratios of the meat of the lambs included will
have similar negative influence on human health.
In contrast with the situation for the PUFA / SFA ratio, ruminant meat has advantages from a human health
viewpoint because it is generally characterized by a low n-6 / n-3 ratio. From a
human health viewpoint, the n-6 / n-3 ratio below 4.0 is required in the diet
(World Health Organization, 2003). According to Simopoulos (2008), a very high
n-6 / n-3 ratio promotes the pathogenesis of many diseases, including
cardiovascular disease, cancer, and inflammatory and autoimmune diseases,
whereas a lower n-6 / n-3 ratio exerts suppressive effects. The analysis
of the n-6 / n-3 ratio was compiled from six studies and altogether included 92 lambs
of the Comisana, Churra Tensinaa,b, Merino Branco, Talaverana and Pramenka
breeds. The overall pooled result for the n-6 / n-3 ratio was 2.22, with a 95 %
CI from 1.95 to 2.49. From the studies included, the ones with Talaverana
and Churra Tensinaa lambs were not within the range of the overall
estimate (Fig. 3c). Talaverana lambs had a significantly lower n-6 / n-3 ratio
(3.16, with a confidence interval from 2.73 to 3.59), while Churra
Tensinaa lambs had a significantly higher n-6 / n-3 ratio (5.04, with a 95 % confidence interval from 3.37 to 6.70). Although Talaverana lambs had
a short starter diet that could influence their n-6 / n-3 ratio, we think that
the main reason for this result is, as in the case of Churra Tensinaa
lambs, the calculation of their ratios. In the studies that included
Talaverana and Churra Tensinaa lambs, n-6 / n-3 ratios were calculated
only from linoleic (C18:2) and α-linolenic (C18:3) fatty acids,
whereas in the other studies these ratios were calculated from a larger
number of acids that belong to the n-6 and n-3 series. This calculation must be treated with caution because the main problem in the papers arises from
the data presented. Cividini et al. (2014) also reported that some of the
authors calculate the main fatty acid proportions and ratios only from the
fatty acids presented in the study, while the others calculate it from the
all fatty acids obtained by the analysis. Therefore, the conclusions drawn from this analysis must certainly take into account calculations of n-6 / n-3 ratios.
Regardless of this and bearing in mind recommendations from the World Health
Organisation (2003), in our analysis only Churra Tensinaa lambs had an n-6 / n-3 ratio that was a little higher (5.04) and that could be negatively related
to human consummation and thus human health.