Oilseed Supplementation Improves Fatty Acid Profile of Milk: Comparison
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Milk is the most consumed dairy product in the world and for humans is one of the major sources of beneficial biocomponents. Lipids from oilseeds can be transferred to milk from cows or converted to other biomolecules with nutraceutical effects, resulting in healthier milk.

  • CLA
  • atherogenic index
  • milk fatty acid
  • experimental design

1. Introduction

The increased consumer concern for the diet–health relationship has increased the attention of nutritionists and animal scientists on the health-beneficial effects of individual foods [1]. Bovine milk is considered as one of the most complete foods with a rich variety of essential nutrients and biocomponents [2]. In this sense, the assessment of milk’s fatty acid (FA) profile has been of great importance in recent decades. Milk fat is the richest natural source of conjugated linoleic acid (CLA), with contents that range from 2 to 53.7 mg g−1 [3]. The wide variability of CLA content can be explained by several factors such as breed, geographical region, and management; however, the most effective strategy to modulate milk’s FA profile is through dietary manipulation [4][5].
Conjugated linoleic acid is made up of a set of positional and geometric isomers of LA (C18:2 c9c12). CLA is an intermediate product in lipid metabolism and ruminal biohydrogenation, and is naturally found in milk and meat from ruminants [6]. CLA is particularly important because various studies using animal models or cell cultures, and some using humans, have found nutraceutical properties in its consumption, such as antiatherogenic [7], antidiabetogenic [8], anticarcinogenic [9][10][11] effects, and that it allows the modification of body composition [12].
The manipulation of diets fed to dairy cows determines variations in the fat profile of milk; for instance, the inclusion of ingredients with higher contents of monounsaturated fatty acid (MUFA) and polyunsaturated fatty acid (PUFA) increases the CLA [13]. Fat supplementation in dairy cow rations is mostly based on fats, oils and oilseeds from vegetable sources. When agro-climatic and economic conditions allow, oilseed supplementation has been widely used and evaluated due to their lower cost, higher UFA content and protein contribution to the ration compared to other strategies such as the use of oils. However, results from studies that have assessed the effect of oilseed inclusion in dairy cow rations have been inconsistent, which can be associated with differences in the methodological and experimental conditions, such as the inclusion level, content of precursors of basal diets and processing of oilseeds and animal variables which could potentially increase milk yield, fat content and FA transfer from oilseeds to milk [14].
Meta-analysis is a cross-disciplinary statistical framework for estimating the average effect associated with a determined intervention factor from several study outcomes under different experimental conditions; additionally, a random-effect model of meta-analysis can be expanded to a mixed-effect model to assess the sources of heterogeneity through meta-regression [15].

2. Milk Yield and Composition

The inclusion of oilseeds in the diet did not affect milk yield due to the isoenergetic balance between diets shown in the great majority of trials, thus not compromising the productive behavior of ruminants [16]. Similarly, Rabiee et al. [17] did not show a statistical difference with the use of oilseeds; however, it can increase milk production with the use of a different source of lipids, where the variation is attributed to the dry matter intake and energy content of the diet. The decrease in milk fat content is affected by the reduction in the action of bacterial fibrolytic enzymes, precursors of acetic fermentation [18], and the production of beta-hydroxybutyrate and some lipogenic enzymes necessary for de novo synthesis in the mammary gland of the main components in milk fat (short- and medium-chain FA) [17][19][20]. Additionally, at the rumen level, UFA has shown toxic effects on some microorganisms [21] by reducing microbial populations and their fermentative activity [22]. Sunflower, cottonseed and soybeans largely led to a reduction in milk fat, which seems to be related to the amount of LA (greater than 50 g 100 g−1 FA), although this is not clear. However, LA is thought to be a substrate in the production of trans isomers, which have been related to milk fat depression syndrome [23]. The supplementation of flaxseed and rapeseed had a lower effect on LA content, which can be associated with the saturation by alternative pathways of their major FA [22], resulting in a lower number of intermediate isomers that inhibit the de novo synthesis of FA in milk fat [23]. In cows, it has been estimated that for every 100 g of fat intake, 0.03% of milk protein is reduced [24]. In thiRes review, we earchers assumed that the substitution of energy ingredients in starch-deficient ruminant diets, such as lipids, affects microbial protein synthesis [19], resulting in a decreased supply and absorption of amino acids in the duodenum, which are required for the formation of milk protein [25]. However, it is possible that milk protein is reduced by the relative decrease in ruminal microorganisms [20][22], caused by the presence of UFA in the rumen [21], which are the main components of the FA structure of the evaluated oilseeds. The obtained heterogeneity for response variables was reduced with the mixed model (meta-regression) in comparison with the random model. Therefore, ourthe results reveal that the used moderating variables covered a considerable proportion of the between-study variation and must be considered in the design of future studies.

3. Milk Fatty Acid Profile

The increase in OA in milk could be due to the contribution of OA, LA and LNA in the diet through oilseeds, where the final step in the rumen is the saturation to stearic FA, but in the mammary gland it is desaturated by the enzyme delta-9 desaturase to OA [17]; it should be remembered that the ruminal biohydrogenation pathway of LNA does not include the direct synthesis of OA [26]. In the same sense, LNA that managed to escape biohydrogenation in the rumen was reflected by the increase in its content in milk [23]. Similarly, an increase in these FA in milk was observed via the supplementation of soybean, rapeseed, sunflower and flaxseed in the diet of cows [27]. In contrast, Akraim et al. [28] achieved a high intake of LNA in dairy cows through linseed, but this FA was not expressed in milk. Vaccenic FA is a biohydrogenation intermediate that is related to the incomplete saturation of LA and LNA [23], the major FA of the oilseeds shown in this review. Theoretically, the presence of LA and LNA in the rumen favors the acceleration of the first step in biohydrogenation and reduces the final saturation step towards stearic FA [29], resulting in an increased flow of the VA into the posterior digestive tract and then into the mammary gland to be secreted into milk [23]. VA is a substrate in de novo synthesis in the mammary gland by delta-9 desaturase enzyme activity to produce CLA [30]. Therefore, the increase in VA is more closely related to greater contents of CLA in milk; this fact could explain the higher levels of CLA in animals supplemented with oilseeds found in the current study. However, the level of response depends on the type of oilseed provided, since the greatest effect size was observed for sunflower seed, soybean and flaxseed, which can be associated with the higher contents of LA and LNA (>57%) in these oilseeds. Additionally, intake of VA increases serum CLA levels in humans [31]; both FA (VA and CLA) have been linked to human health with decreased chronic diseases [32], and the intake of CLA and VA has been shown to lead to a reduction in coronary heart disease, low incidence of atherosclerosis [33], decreased risk of hypertension [34], low risk of type II diabetes mellitus [35] and decreased obesity [36]; in addition, CLA has been attributed to reducing cancer induced in laboratory animals [10], and has great potential to improve menopausal symptoms, bone health, sarcopenia and sarcopenic obesity [37]. Including oilseeds in the diet of cows reduces the content of SFA in milk and increases the concentration of UFA, possibly by decreasing the production of volatile fatty acid (VFA) in the rumen, specifically acetic acid, the main substrate for the de novo synthesis of short- and medium-chain SFA [38]. Propionic acid production can be affected by the substitution of starchy energy ingredients and/or non-structural carbohydrates in the diet [39]. The use of oilseeds in ruminant diets can increase propionic acid production and decrease acetic acid production proportionally. This is because of the release of glycerol from triglycerides in lipolysis [40]. This alteration in the rumen ratio of acetic to propionic acids does not affect milk yield but creates the conditions (mainly rumen pH and/or microbial population) for increased UFA content [41]. Long-chain PUFA that escape from biohydrogenation are absorbed by the intestine and increase the ratio of UFA in milk at the expense of a decrease in SFA [16], which may be conditioned by an inhibitory effect of acetyl-CoA carboxylase and fatty acid synthetase enzymes at the mammary gland level [42]. The importance of increasing the proportion of PUFA in milk resides in the fact that human consumption of PUFA can reduce obesity and mortality from cardiovascular problems by up to 30% and decreases the incidence of diabetes by up to 50% [43]; the omega-3 PUFA showed a 20% reduction in mortality in patients with cardiac problems [44]. OurThe reviewsults showed a 62% increase in omega-3 PUFA in cow’s milk with the inclusion of oilseeds as a dietary supplement. In this regard, extruded and ground whole oilseeds showed the greatest effect, possibly due to the greater availability of these PUFA that have escaped ruminal biohydrogenation by being absorbed by the small intestine and secreted in milk; although, the pericarp of these oilseeds plays an important role in the protection of UFA by limiting biohydrogenation [22]. The AI proposed by Ulbricht and Southgate [45] is the sum of hypercholesterolemic SFA content divided by the sum of protective UFA. A low AI reflects milk with a low SFA content [46]; therefore, the consumer reduces the risk of fat contributing to the development of atheroma [47]. In this sense, ithis review is demonstratesd that there is an adequate relation between the biocomponents of milk produced by cows supplemented with oilseeds, i.e., FA profile, and so can be considered as a functional food with benefits on the human health. However, the milk composition and the FA profile showed a high variability between studies in response to oilseed supplementation. Therefore, considering the role of covariates through meta-regression analysis is a fundamental step to provide a full understanding of the oilseed supplementation strategy in dairy cows.

4. Meta-Regression

OurThe results showed a higher milk fat content in Jersey cows; however, these findings must be cautiously considered due to the reduced number of studies available in this breed. The higher milk fat content found in Jersey cows compared to that of Holstein could be associated with the higher concentration of SFA (lauric, myristic, palmitic, and stearic) and UFA (LA) in Jersey compared to Holstein cows [48]. Carroll et al. [49] suggest that the differences in fat content between cow breeds is associated with the expression and activity of acetyl-CoA carboxylase and mammary stearoyl CoA desaturase, which are responsible of FA and UFA synthesis, respectively. Additionally, several authors reported a positive relationship between the diameter of the milk fat globule and fat content [50][51]. In this sense, the size of the milk fat globule can be explained partly by the greater fat content in Jersey cow´s milk, supported by the fact that fat globules more than 50 mm in diameter are more numerous in Jersey than Holstein cows by a factor of 50 [49]. The composition of cow’s milk changes with the lactation stage [52]. The meta-regression showed an effect of the lactation stage on the response level to oilseed supplementation of some milk components. The response in terms of milk protein to the intervention factor was higher at the beginning and the end of lactation, possibly due to the amount of milk produced [53]. On the other hand, the effect size of oilseed supplementation with regard to fat content was larger when the experimental period was performed in the second stage of lactation, which can be explained by the stronger relationship between energy balance and milk fat synthesis. During the second stage of lactation, after the peak of lactation, there is an increase in dry matter intake, leading to an increased energy supply used for de novo milk fat synthesis [54]. With regard to the negative relationship observed in UFA (LNA and oleic acid) from experiments carried out in the third stage of lactation, ourthe results are in agreement with Stoop et al. [52], who reported a lower content of C18 FA and high proportion of short- and medium-chain FA (C6:0 to C14:0) in milk towards the third stage of lactation. This fact could explain the negative effect of AI in this lactation stage. The high LA content of sunflower seed (60.4% of FA) affected milk fat content. Supplementing with PUFA-rich sources reduces acetic and butyric fermentation in the rumen and consequently decreases de novo synthesis in the mammary gland and inhibits lipogenic enzymes [55]. Contrary to this, the addition of sunflower to cow diets has a positive effect on the OA content, possibly due to the FA that escape ruminal biohydrogenation and are absorbed by the small intestine to be secreted in milk and/or by the action of the enzyme delta-9 desaturase that has its action in the mammary gland [17]. Additionally, the inclusion of rapeseed and soybean in dairy cow rations results in a positive relationship with the OA content, which can be associated with the fact that these oilseeds have a high concentration of this FA (54.6 g and 22.9 g 100 g−1 FA). Additionally, Sterk et al. [56] found a positive relationship with regard to LA content between diet and milk. Thus, the type of oilseed used in cow diets provide the substrates for the different contents of FA in the milk produced and therefore also influences the level of response to supplementation. The inclusion of rich sources of PUFA in the diet of ruminants has shown increases in the concentration of omega-3 PUFA in meat and milk [14][57]. The type and source of PUFA consumed by the animal can have different impacts on microbial populations and rumen fermentation [58]. These adverse effects of PUFA may be amplified through the use of vegetable oils in the diet compared to oilseeds [59]. Studies using sunflower oil [60] and soybean oil [61] in the diet of dairy cattle reflected an increased concentration of OA in milk, as well as a reduction in short- and medium-chain SFA (C10:0-C16:0). The decrease in VA in milk fat with dietary supplementation of sources of OA, LA and LNA (majority FA in rapeseed, soybean and linseed) could be explained by the decreased synthesis of VA in the ruminal biohydrogenation of PUFA; the level of supplementation was not sufficient to show an effect on this FA and there was a complete biohydrogenation of OA, LA and LNA to stearic FA. The interactions between the type of oilseed and level of inclusion show that the highest levels of response to oilseed supplementation were reached with inclusions of 15% of DM of linseed and 6–7% of DM of rapeseed. The grinding process exposes the oilseeds’ FA to biohydrogenation in the rumen, being the most affected the UFA and omega-3 PUFA [22], which is in accordance with the results of the current study; however, some FA such as LA can escape the biohydrogenation process, and hence reach the mammary gland [23]. Additionally, as explained above, the OA may escape this hydrogen saturation in the rumen and/or be desaturated from stearic FA in the mammary gland. The unprocessed oilseeds have a negative effect on dry matter intake, thus promoting a decrease in milk yield [62] with increases (β = 0.21; p < 0.05) in milk fat content. Unprocessed oilseeds have a negative effect on UFA and positive one on SFA, which may be due to a slower passage rate which allows the rumen microorganisms to saturate PUFA and MUFA of oilseeds [18]. The pericarp of whole oilseeds reaching the small intestine does not allow the absorption of the contained FA [22]. In this sense, the positive effect of SFA and negative effect of UFA with this supplementation strategy (whole oilseed) impacts on a higher AI, which is related to the higher content of SFA and therefore a less positive human-health effect [63][64]. Roasted oilseeds (whole and ground) are better utilized by ruminants [65], but in ourthe reviewsearch only had a positive effect on omega-6 PUFA, LA and OA, like the results reported by Rafiee-Yarandi et al. [66], which may be related to changes in structural components that increase the level of protection of FA to ruminal biohydrogenation to some degree [19]. On the other hand, total UFA are affected, especially omega-3 PUFA, which may be due to the increased instability of these FA with the heat of cooking. This effect on UFA (omega-3) resulted in a higher AI, which is undesirable in cow’s milk; however, the type of oilseed to be roasted should be considered; for example, including roasted ground soybeans in the diet of cows resulted in a higher UFA content and lower SFA content, having a lower AI, therefore producing healthier milk [64]. Milk’s fat content and FA composition are strongly affected by the fiber content and F:C ratio. The increasing of the F:C ratio is a strategy to increase the levels of PUFA in milk [67], as is revealed in the meta-analysis carried out by Angeles-Hernandez et al. [68], who reported higher levels of milk fat (>0.32 g 100 g−1) and CLA content (>2.28 g 100 g−1 FA) in diets with an inclusion of at least 40% DM of forage. Additionally, the consumption of appropriate of levels of high-quality forage to allow the rumen functions to be maintained under optimal conditions [23][69]. From another perspective, diets with a low F:C ratio, and associated with a ruminal pH below 6.0, reduce PUFA biohydrogenation, resulting in alternative routes and changes in the production of biohydrogenation intermediates [67]. In relation to the intervention factor assessed in the current work esearch (oilseed supplementation), an interaction between the F:C ratio and the response to the supplementation of oil sources was reported by Palmquist and Jenkins [18]. Additionally, Ueda et al. [55] observed a significant interaction between a high forage or high concentrate ratio in the diet and flaxseed oil supplementation on ruminal digestion. The above-mentioned studies support the role of the forage-inclusion level covariate as the source of between-study variability. The significate interaction of this covariate was attributed to the CLA, Σ omega-6, and SFA outcomes. This significant relationship can be explained by the fact that the PUFA-rich oil supplementation decreased de novo synthesis in the mammary gland, which can be associated with the reduction in the synthesis of acetate and butyrate, or with the changing in the hydrogenation pathway generating FA with the subsequent inhibition of lipogenic enzymes [55]. Certainly, Castro et al. [70] assumed a reduced lipogenic activity in the mammary gland due to the effect of the addition of PUFA-rich sources in the diet with mixtures of conserved forages, which is reflected in the lower total fat content in milk compared to the control; in addition, the CLA content in milk was lower with the supplementation of LA compared to LNA, due to the inclusion of soybean and flaxseed oil in the diet, respectively. With respect to CLA synthesis in the mammary gland, the activity of the enzyme delta-9 desaturase is highly correlated with VA content [71]. However, changes in rations, by manipulating the F:C ratio or oil intake, cause modifications in the microbial population, which could alter the ruminal biohydrogenation of MUFA and PUFA, promoting the synthesis of specific isomers, which alters the availability of VA by the mammary gland [23]. In accordance with ourthe findings, the level of NDF of diets affects the response to oil supplementation to fat content, OA and UFA outcomes. In this sense, Sterk [72] stated that the NDF content of the diet affects the UFA in milk content, but the degree of affectation is dependent on the form of supplementation of rich sources of FA in the diet. The effect of dietary NDF content on the UFA content in milk is more negative when the source of UFA in the diet is in free oil form, in contrast to the protected form [72]. A low dietary fiber content is related to less complete biohydrogenation [59], which would explain the higher proportion of UFA in milk fat. Additionally, the same authors [72] indicated that the effect of NDF content depends on the type of main forage in the diet and the UFA content of the diet. The milk FA profile is a product of the manipulation and interaction of a set of factors such as: diet composition, feed intake, ruminal fermentation pattern, lipid metabolism in the liver, body fat mobilization, ruminal biohydrogenation and bacterial degradation of FA and synthesis and absorption of FA in rumen and mammary glands [52][53]. WResearchers therefore suggest that these factors (almost the same as those reported in the current study) must be considered at the farm and industry levels in the design of feed strategies and in the research process to reduce the noise effect, taking into account the role of these factors as covariates when it is possible. The cross-over design determined the allocation of two or more treatments to the same experimental unit but in different periods. In this sense, there should be no carry-over or lasting effect for the previous treatment. Hence, the purpose of wash-out periods is to eliminate the effect of the previous treatment [73]. OurThe result revealed significant effects of the experimental design and length of wash-out periods on some of the milk components, mainly those associated with the FA profile. OurThe meta-regression results revealed that the response to oilseed supplementation decreases as the number of wash-out days increases to LN, OA VA, CLA and UFA outcomes, which could elucidate a possible cumulative effect of previous treatment in the cross-over design when the wash-out period is short. Therefore, to define the duration of wash-out periods, the variable response and nature of the treatment must be taken into account [74]. According to ourthe results, cross-over experiments designed to evaluate the effect of oilseed inclusion on milk composition must consider a minimum wash-out period of 20 days to avoid a type I error.

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