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Laboratory for Animal Nutrition and Animal Product Quality (Lanupro), Department of Animal Sciences and Aquatic Ecology, Ghent University, 9000 Gent, Belgium
* Research Group Marine Biology, Department of Biology, Ghent University, Belgium
B. Vlaeminck
Footnotes
* Research Group Marine Biology, Department of Biology, Ghent University, Belgium
Affiliations
Laboratory for Animal Nutrition and Animal Product Quality (Lanupro), Department of Animal Sciences and Aquatic Ecology, Ghent University, 9000 Gent, Belgium
Laboratory for Animal Nutrition and Animal Product Quality (Lanupro), Department of Animal Sciences and Aquatic Ecology, Ghent University, 9000 Gent, Belgium
To meet the energy requirements of high-yielding dairy cows, grains and fats have increasingly been incorporated in ruminant diets. Moreover, lipid supplements have been included in ruminant diets under experimental or practical conditions to increase the concentrations of bioactive n-3 fatty acids and conjugated linoleic acids in milk and meat. Nevertheless, those feeding practices have dramatically increased the incidence of milk fat depression in dairy cattle. Although induction of milk fat depression may be a management tool, most often, diet-induced milk fat depression is unintended and associated with a direct economic loss. In this review, we give an update on the role of fatty acids, particularly originating from rumen biohydrogenation, as well as of rumen microbes in diet-induced milk fat depression. Although this syndrome seems to be multi-etiological, the best-known causal factor remains the shift in rumen biohydrogenation pathway from the formation of mainly trans-11 intermediates toward greater accumulation of trans-10 intermediates, referred to as the trans-11 to trans-10 shift. The microbial etiology of this trans-11 to trans-10 shift is not well understood yet and it seems that unraveling the microbial mechanisms of diet-induced milk fat depression is challenging. Potential strategies to avoid diet-induced milk fat depression are supplementation with rumen stabilizers, selection toward more tolerant animals, tailored management of cows at risk, selection toward more efficient fiber-digesting cows, or feeding less concentrates and grains.
Farm animals have been undergoing human-managed selection since their original domestication. In the last 60 yr, breeding programs have focused on the genetic improvement of production traits, such as milk yield of dairy cows (
). Moreover, lipid supplements have been included in ruminant diets under experimental, as well as practical conditions, to increase the concentrations of bioactive n-3 fatty acids (FA) and CLA in milk and meat (
) and enhance cows' reproductive performance. However, such feeding practices might increase the incidence of diet-induced milk fat depression (MFD) in dairy cattle (
Diets supplemented with starch and corn oil, marine algae, or hydrogenated palm oil differentially modulate milk fat secretion and composition in cows and goats: A comparative study.
In the following sections, we will provide background of diet-induced MFD, beginning with its definition, and give an update on the role of rumen biohydrogenation intermediates in MFD since the review of
, based on recent studies in which associations were investigated between rumen or milk FA and decreases in milk fat. Furthermore, this review also provides a summary of the role of rumen microbes in MFD, based on pure culture studies and recent insights provided by molecular techniques. Finally, potential strategies to reduce the risk of MFD are discussed. Although this review particularly focuses on diet-induced MFD in dairy cows, differences and similarities between the response of cattle and small ruminants to diets associated with MFD will also be discussed.
Data used in the linear regression analysis of this review were derived from publications found via Google Scholar using the key words “milk fat depression,” “milk fatty acid,” and “rumen fermentation,” published between 2008 and 2018. To investigate the effects of specific traits (i.e., rumen pH, rumen proportion of acetate or propionate, milk fat proportion of trans-10,cis-12 CLA or trans-10 18:1) on milk fat content or yield, a linear regression analysis was done using the MIXED procedure of SAS (version Enterprise Guide 7.1; SAS Institute Inc., Cary, NC) with the respective traits as independent variables (fixed effects) and study as a random effect (
). When the data suggested an exponential curve, a natural log-transformation was performed before linear regression analysis.
WHAT IS MFD?
Diet-induced MFD in dairy cattle is classically characterized by a reduction in milk fat content and yield with concomitant changes in ruminal biohydrogenation pathways, with no change in milk yield or in the yield of other milk components (
). Accordingly, this definition excludes situations with impaired milk fat yield resulting from lower milk yield, such as that due to decreased energy intake. However, there is some diversity in diet-induced MFD phenotypes, which implies that some MFD conditions do not neatly fit in this classical definition. Indeed, in some studies with fish oil supplementation (
), decreases in milk fat concentrations were also accompanied by reduced milk fat synthesis and lower total milk yield. An increase in milk yield has even been described in ewes receiving fish oil, but associated downregulation of key genes involved in the mammary lipogenesis process confirmed nutrigenomic mechanisms rather than a milk dilution factor being responsible for the reduction in milk fat concentration (
). Whether they fit in the classical definition of MFD or not, the common feature of diet-induced MFD conditions is the alteration in ruminal biohydrogenation pathways, which usually includes the well-known trans-11 to trans-10 shift (
Zened, A., A. Meynadier, L. Cauquil, J. Mariette, C. Klopp, S. Dejean, I. Gonzalez, O. Bouchez, F. Enjalbert, and S. Combes. 2016. Trans-11 to trans-10 shift of ruminal biohydrogenation of fatty acids is linked to changes in rumen microbiota. (Abstr.) P-202 (pp. 150). Gut Microbiology 2016: Proceedings of the 10th Joint Symposium on Gut Microbiology; 2016 June 20–23; Clermont-Ferrand, France.
Distinct blood and milk 18-carbon fatty acid proportions and buccal bacterial populations in dairy cows differing in reticulorumen pH response to dietary supplementation to rapidly fermentable carbohydrates.
). These alterations in ruminal lipid metabolism are accompanied by changes in milk FA toward a reduced proportion and yield of short- and medium-chain FA, whereas proportions of longer-chain FA increase, although their yield usually remains constant or is decreased (
Induction of and recovery from milk fat depression occurs progressively in dairy cows switched between diets that differ in fiber and oil concentration.
). The few situations in which preformed FA uptake seemed to be more strongly affected than de novo FA synthesis (on a molar basis) were associated with marine lipid supply in the diet (
Dietary marine algae (Schizochytrium sp.) increases concentrations of conjugated linoleic, docosahexaenoic and transvaccenic acids in milk of dairy cows.
Effects of abomasal infusion of conjugated linoleic acids, Sterculia foetida oil, and fish oil on production performance and the extent of fatty acid Δ9-desaturation in dairy cows.
Although induction of MFD occasionally may be a management tool, as in some situations of negative energy balance and in markets where milk production is regulated by a quota system based on milk fat (
), most often, diet-induced MFD is unintended and is more frequently perceived as being clearly negative. This decrease in milk fat synthesis not only results in a direct economic loss, but is also associated with a reduction in feed conversion efficiency (
The effect of marine algae in the ration of high-yielding dairy cows during transition on metabolic parameters in serum and follicular fluid around parturition.
Effects of dietary fatty acids and carbohydrates on the ratio of serum total to HDL cholesterol and on serum lipids and apolipoproteins: A meta-analysis of 60 controlled trials.
). Indeed, under MFD conditions, a shift occurs in milk FA profile from trans-11 18:1 as the major trans FA toward increased proportions of trans-10 18:1 (
). Epidemiological studies indicated that industrial trans FA, which are also enriched in trans-10 18:1, have a negative effect on serum cholesterol and lipoprotein metabolism, thereby increasing the risk for coronary heart disease (
). Nevertheless, to the best of our knowledge, no human intervention study has been performed with trans-10 18:1-containing milk (or dairy products), and only 2 animal studies have compared milk or butter enriched in trans-10 18:1 or trans-11 18:1.
Butters rich either in trans-10-C18:1 or in trans-1-C18:1 plus cis-9, trans-11 CLA differentially affect plasma lipids and aortic fatty streak in experimental atherosclerosis in rabbits.
observed increased total cholesterol and low-density lipoprotein cholesterol concentrations in plasma and increased lipid deposition in the aorta of rabbits supplemented with trans-10 18:1 compared with trans-11 18:1-enriched butter. Furthermore, plasma triacylglycerides concentrations tended to increase in rats treated with trans-10 18:1-enriched milk fat, whereas milk fat containing trans-11 18:1 and cis-9,trans-11 CLA provoked the opposite (
). Although those animal studies showed a potential negative risk of trans-10 18:1-containing dairy products for human health, extrapolation of findings from animal studies to humans has to be made with caution. Some feeding strategies that increase trans-10 18:1 proportion in dairy products may induce larger increments in trans-11 18:1 and cis-9,trans-11 CLA or other bioactive FA that counteract the potentially negative effects of trans-10 18:1, as suggested in a hamster model (
Butter naturally enriched in conjugated linoleic acid and vaccenic acid alters tissue fatty acids and improves the plasma lipoprotein profile in cholesterol-fed hamsters.
). As such, further research is required to evaluate the effects of milk from animals under extreme MFD conditions on human health. Above this human health consequence, MFD is often associated with modified ruminal fermentation and frequently considered an indicator for impaired animal health (i.e., ruminal acidosis) and reduced ruminal efficiency (
), thereby detrimentally affecting animal welfare. Hence, MFD is an undesirable situation both from an economic perspective, as well as from an animal welfare and human health perspective.
DIETS ASSOCIATED WITH MFD
Diets causing MFD can be divided into 2 broad groups: (1) diets rich in rapidly fermentable carbohydrates (RFCH), low in physically effective fiber (peNDF), or both, and (2) diets supplemented with UFA, especially marine lipids containing eicosapentaenoic acid (EPA, 20:5n-3) and docosahexaenoic acid (DHA, 22:6n-3;
Increasing the fermentability of a cow's diet has been frequently used to meet the high energy requirements of high-yielding dairy cows. Nevertheless, increasing the fermentability of the diet does not only increase the milk production, but it also affects the rumen environment, potentially inducing MFD. The most common type of diet within this group is a high-grain/low-forage diet, particularly when rapidly fermentable starch sources are employed, such as wheat grain or high-moisture corn (
). However, diets in which the fiber content is adequate but the peNDF content is inadequate (e.g., a pelleted fiber source, such as pelleted alfalfa) could fall into this group because of the rapid fermentation of these fiber sources, which reduces the ability to maintain normal rumen function (
). Young pastures contain a significant amount of UFA, in addition to high concentrations of sugars and soluble fiber, resulting in a low peNDF content. Selection by grazing cows against the fiber content (
Changes in the botanical composition and nutritive characteristics of pasture, and nutrient selection by dairy cows grazing rainfed pastures in western Victoria.
) might decrease the relative intake of peNDF even more. Furthermore, diet fermentability may interact with other ingredients of the ration, and feeding rapidly fermentable diets together with PUFA-rich supplements from plant sources, soybean, and sunflower, is known to increase the risk of MFD (
Diet-induced milk fat depression is associated with alterations in ruminal biohydrogenation pathways and formation of novel fatty acid intermediates in lactating cows.
). On the other hand, literature on this topic suggests that RFCH diets with or without plant lipids inhibit de novo FA synthesis but rarely impair total milk fat synthesis in small ruminants (
Effects of feeding oilseeds rich in linoleic and linolenic fatty acids to lactating ewes on cheese yield and on fatty acid composition of milk and cheese.
Effect of level and type of starchy concentrate on tissue lipid metabolism, gene expression, and milk fatty acid secretion in Alpine goats receiving a diet rich in sunflower oil.
). These results may be explained by the ability of small ruminants to counteract the inhibition in de novo FA synthesis by concomitant increments in preformed FA secretion (
Distinct blood and milk 18-carbon fatty acid proportions and buccal bacterial populations in dairy cows differing in reticulorumen pH response to dietary supplementation to rapidly fermentable carbohydrates.
). Furthermore, data from 28 studies in dairy cows (Figure 1A, B) show that rumen pH is related to neither milk fat content (r2 = 0.190) nor milk fat yield (r2 = 0.070). This suggests that a low rumen pH is not the main determinant of MFD.
Figure 1Relationship between milk fat content (MFC; A, C, E) or yield (MFY; B, D, F) and rumen pH (A, B), proportion (mol/1,000 mol of VFA) of acetate (C, D), or propionate (E, F). Square = milk fat content; triangle = milk fat yield. Data derived from 28 studies (
Effect of lauric acid and coconut oil on ruminal fermentation, digestion, ammonia losses from manure, and milk fatty acid composition in lactating cows.
Effect of replacing solvent-extracted canola meal with high-oil traditional canola, high-oleic acid canola, or high-erucic acid rapeseed meals on rumen fermentation, digestibility, milk production, and milk fatty acid composition in lactating dairy cows.
Interaction of molasses and monensin in alfalfa hay- or corn silage-based diets on rumen fermentation, total tract digestibility, and milk production by Holstein cows.
Effects of partially replacing barley silage or barley grain with dried distillers grains with solubles on rumen fermentation and milk production of lactating dairy cows.
Supplementation of increasing amounts of linseed oil to dairy cows fed total mixed rations: Effects on digestion, ruminal fermentation characteristics, protozoal populations, and milk fatty acid composition.
Linseed oil supplementation to dairy cows fed diets based on red clover silage or corn silage: Effects on methane production, rumen fermentation, nutrient digestibility, N balance, and milk production.
Replacing alfalfa silage with corn silage in dairy cow diets: Effects on enteric methane production, ruminal fermentation, digestion, N balance, and milk production.
The effect of buffering dairy cow diets with limestone, calcareous marine algae, or sodium bicarbonate on ruminal pH profiles, production responses, and rumen fermentation.
Effect of dietary starch concentration and fish oil supplementation on milk yield and composition, diet digestibility, and methane emissions in lactating dairy cows.
Reduced-fat dried distillers grains with solubles reduces the risk for milk fat depression and supports milk production and ruminal fermentation in dairy cows.
Short communication: Forage particle size and fat intake affect rumen passage, the fatty acid profile of milk, and milk fat production in dairy cows consuming dried distillers grains with solubles.
Rumen fermentation, methane concentration and fatty acid proportion in the rumen and milk of dairy cows fed condensed tannin and/or fish-soybean oils blend.
Considering the importance of acetate as a carbon source for milk fat synthesis and the observed shift in the rumen VFA profile toward less acetate and more propionate with diets rich in RFCH, low in peNDF, or both, acetate deficiency or propionate overflow might induce MFD.
reviewed the acetate deficiency theory and concluded there was little support for it. However, more recent articles have renewed the interest in the potential effect of shifts in VFA on mammary lipogenesis. For example,
observed increased milk fat yield (+90 g/d) and concentration (+0.2 percentage units) upon dietary supplementation with sodium acetate at 2.9% of diet DM. In the study by
, ruminal infusion of 800 g/d of propionate to dairy cows reduced the milk fat content and yield by 7.8 and 9.8%, respectively (mainly through changes in preformed FA), whereas ruminal infusion of the same amount of acetate increased the milk fat content by 6.5% (mainly through promotion of de novo FA synthesis). Nevertheless, data from 28 recent studies (Figure 1C–F and Supplemental Figure S1; https://doi.org/10.3168/jds/2019-17662) revealed that rumen proportions of acetate or propionate do not affect milk fat content or yield (r2 ≤ 0.118). Although these studies relied on acetate and propionate proportions rather than productions, the lack of any relation suggests that shifts in rumen VFA, induced by increasing RFCH, are not a major cause of the associated reductions in milk fat content and yield. Moreover, the decrease in milk fat content provoked by propionate infusion (
Induction of and recovery from milk fat depression occurs progressively in dairy cows switched between diets that differ in fiber and oil concentration.
Effect of feeding linseed oil in diets differing in forage to concentrate ratio: 1. Production performance and milk fat content of biohydrogenation intermediates of a-linolenic acid.
Diet-induced milk fat depression is associated with alterations in ruminal biohydrogenation pathways and formation of novel fatty acid intermediates in lactating cows.
Effects of ruminal or duodenal supply of fish oil on milk fat secretion and profiles of trans-fatty acids and conjugated linoleic acid isomers in dairy cows fed maize silage.
Effect of dietary starch concentration and fish oil supplementation on milk yield and composition, diet digestibility, and methane emissions in lactating dairy cows.
Fish oils and lipids from marine mammals and marine algae are characterized by the presence of 2 PUFA: EPA and DHA. Marine lipids have been added to ruminant diets in an attempt to increase the concentrations of human health–promoting PUFA in milk and meat (
). Indeed, supplementation with products enriched in EPA and DHA to dairy cows resulted in lower rumen concentrations of SFA, whereas the concentrations of MUFA and PUFA increased (
Effect of extruded linseeds alone or in combination with fish oil on intake, milk production, plasma metabolite concentrations and milk fatty acid composition in lactating goats.
), which is a neutral FA in regard to human health. Nevertheless, the increase in UFA might be positive, as several UFA have been shown to beneficially affect human health. For example, n-3 PUFA, such as EPA, DHA, and 18:3n-3, play a beneficial role in the prevention of cardiovascular disease (
). Furthermore, cis-9,trans-11 CLA and trans-10,cis-12 CLA have been shown to affect immune function and to have protective effects against cancer, obesity, diabetes, and atherosclerosis (
). Although the dietary intake of those health-promoting UFA through milk is low, preventive benefits of milk consumption against several diseases have been described (
). In contrast to interspecies differences in the response to high RFCH/low peNDF diets, marine lipid-induced MFD has consistently been described in bovine, ovine, and caprine, indicating that the underlying mechanisms of the 2 MFD types might differ (
Individual variation of the extent of milk fat depression in dairy ewes fed fish oil: Milk fatty acid profile and mRNA abundance of candidate genes involved in mammary lipogenesis.
Diets supplemented with starch and corn oil, marine algae, or hydrogenated palm oil differentially modulate milk fat secretion and composition in cows and goats: A comparative study.
). Indirect comparisons among studies in the literature tended to suggest that goats and sheep were less prone than cattle to detrimental effects of marine lipids on mammary lipogenesis (
Effect of extruded linseeds alone or in combination with fish oil on intake, milk production, plasma metabolite concentrations and milk fatty acid composition in lactating goats.
). Nevertheless, the type of basal diet might play a role. The forage in the ration of small ruminants is usually hay or grass silage, whereas lactating dairy cows often receive maize silage. When cows and goats were fed exactly the same basal diet (i.e., grass hay and concentrates) in direct comparative studies, similar milk fat responses were observed after marine lipid supplementation (
Diets supplemented with starch and corn oil, marine algae, or hydrogenated palm oil differentially modulate milk fat secretion and composition in cows and goats: A comparative study.
Milk fat depression in dairy ewes fed fish oil: Might differences in rumen biohydrogenation, fermentation, or bacterial community explain the individual variation?.
), resulting in a shortage of 18:0 (melting point = 69.7°C) for mammary uptake that would constrain the synthesis of cis-9 18:1 (melting point = 16.0°C) by Δ9-desaturation (
Effects of ruminal or duodenal supply of fish oil on milk fat secretion and profiles of trans-fatty acids and conjugated linoleic acid isomers in dairy cows fed maize silage.
; LipidBank database, http://www.lipidbank.jp, Japanese Conference on the Biochemistry of Lipids). These alterations in milk FA profile upon marine oil supplementation, which have been described across ruminant species (
Diets supplemented with starch and corn oil, marine algae, or hydrogenated palm oil differentially modulate milk fat secretion and composition in cows and goats: A comparative study.
). An extension of the biohydrogenation theory postulated that increased milk fat melting point may impair the capacity to achieve an adequate fluidity for milk fat secretion, which might account for this type of MFD (
, challenging the theory of a shortage of 18:0. Surprisingly, the combination of fish oil and 18:0 further aggravated the trans-10 shift in biohydrogenation pathways compared with the addition of fish oil alone (
). Also in cows, supplementation of a blend of fish oil in combination with either a fat rich in 18:0 or a plant oil high in linolenic acid oil resulted in similar responses in milk fat concentration and yield, as well as ruminal trans-10 18:1 proportions (
Supplementation of increasing amounts of linseed oil to dairy cows fed total mixed rations: Effects on digestion, ruminal fermentation characteristics, protozoal populations, and milk fatty acid composition.
Effect of dietary fish oil supplements alone or in combination with sunflower and linseed oil on ruminal lipid metabolism and bacterial populations in lactating cows.
Milk fat depression in dairy ewes fed fish oil: Might differences in rumen biohydrogenation, fermentation, or bacterial community explain the individual variation?.
observed lower acetate concentrations in rumen fluid of sheep displaying strong MFD compared with sheep showing mild MFD, upon dietary supplementation with 2% fish oil. Trials conducted in bovine and caprine animals (in vitro and in vivo) have also shown marine lipid-induced reductions in ruminal acetate concentrations and decreases in acetate:propionate ratio (
). Perhaps, shifts in VFA and putative consequences on de novo synthesis and preformed FA uptake play a more important role in marine lipid-induced MFD compared with RFCH-induced MFD, which warrants additional and targeted research. Results from recent studies would also recommend re-evaluating the relevance of the inhibition in preformed FA uptake in marine lipid-induced MFD (
Effects of abomasal infusion of conjugated linoleic acids, Sterculia foetida oil, and fish oil on production performance and the extent of fatty acid Δ9-desaturation in dairy cows.
Individual variation of the extent of milk fat depression in dairy ewes fed fish oil: Milk fatty acid profile and mRNA abundance of candidate genes involved in mammary lipogenesis.
The biohydrogenation theory established that diet-induced MFD involves an interrelationship between rumen digestive processes and mammary tissue metabolism (
). Diets known to induce MFD alter rumen biohydrogenation pathways of dietary PUFA toward the formation of specific FA intermediates. After absorption in the duodenum and transfer to the mammary gland via the blood stream, some of those biohydrogenation intermediates might inhibit milk fat synthesis. First, the ruminal metabolism of dietary lipids will briefly be explained. Second, a short overview will be given of the main rumen biohydrogenation pathways, after which the association between specific biohydrogenation intermediates and MFD will be discussed in more detail.
Lipid Metabolism in the Rumen
The diet of lactating dairy cows typically contains 4 to 5% crude fat (on a DM basis), corresponding to about 2.3 to 2.5% total FA (
). Primary sources of lipid in the ruminant diet are forages and concentrates, which mainly contain 18-carbon UFA (i.e., α-linolenic acid, 18:3n-3; linoleic acid, 18:2n-6; and oleic acid, cis-9 18:1;
). However, the lipid content can be increased by the use of fat supplements. The major lipid class of forages is glycolipids, whereas the majority of lipids in concentrates is present in the form of triacylglycerides. Following ingestion, dietary lipids are hydrolyzed, and the nonesterified FA are released into the rumen. Then, 18:3n-3, 18:2n-6, and cis-9 18:1 are converted to SFA via a cis-trans isomerization to trans FA intermediates, followed by hydrogenation of the double bonds (
Numerous in vivo and in vitro studies have enabled several ruminal biohydrogenation pathways of 18:2n-6, 18:3n-3, and cis-9 18:1 to be elucidated. Under normal rumen conditions, 18:2n-6 is mainly isomerized to cis-9,trans-11 CLA, which is further hydrogenated to trans-11 18:1 and ultimately to 18:0 (Figure 2). The major biohydrogenation pathway of 18:3n-3 involves cis-9,trans-11,cis-15 conjugated linolenic acid (CLnA), trans-11,cis-15 18:2 and trans-11 18:1 as intermediates (Figure 3), whereas the major part of cis-9 18:1 is directly hydrogenated to 18:0 in the rumen (Figure 4). However, ruminal biohydrogenation of 18:2n-6, 18:3n-3, and cis-9 18:1 might also result in the formation of several other minor FA intermediates, such as trans-9,trans-11 CLA, trans-10 18:1, and cis-12 18:1 (Figure 2–4). In addition to the pathways shown in Figures 2–4, alternative pathways might exist, as supported by the identification of additional biohydrogenation intermediates in recent in vitro experiments using stable isotopes in cows (deuterium oxide;
). Arrows with solid lines highlight the major biohydrogenation pathway, and arrows with dashed lines describe the formation of minor intermediates, under physiologically normal conditions in the rumen.
). Arrows with solid lines highlight the major biohydrogenation pathway, and arrows with dashed lines describe the formation of minor intermediates, under physiologically normal conditions in the rumen.
). Arrows with solid lines highlight the major biohydrogenation pathway, and arrows with dashed lines describe the formation of minor intermediates, under physiologically normal conditions in the rumen.
). However, the reduction of unsaturated 18-carbon FA to 18:0 in the rumen is incomplete, and numerous 18:1, 18:2, and 18:3 intermediates accumulate. Diets known to induce MFD would often result in greater amounts of particular 18:1 intermediates and minor amounts of 18:2 and 18:3 intermediates escaping the rumen compared with normal situations. Plant lipids rich in C18 UFA provide the substrates for the direct increase in 18:1 production in the rumen (
). As mentioned above, dietary supplementation of marine lipids rich in EPA and DHA consistently inhibited the final biohydrogenation step to 18:0 in cows, sheep, and goats (
Dietary fish oil supplements modify ruminal biohydrogenation, alter the flow of fatty acids at the omasum, and induce changes in the ruminal Butyrivibrio population in lactating cows.
Effect of dietary oil sources on fatty acid composition of ruminal digesta and populations of specific bacteria involved in hydrogenation of 18-carbon unsaturated fatty acid in finishing lambs.
), resulting in the indirect accumulation of 18:1 isomers, although other steps may also be affected. Additionally, in this case, some biohydrogenation intermediates of very long-chain PUFA with 20 or 22 carbons are accumulating. Moreover, decreases in rumen pH below 6.0 lowered the extent of 18:2n-6 and 18:3n-3 isomerization and inhibited the final reduction to 18:0 in vitro in cattle (
Induction of and recovery from milk fat depression occurs progressively in dairy cows switched between diets that differ in fiber and oil concentration.
using a canonical discriminant analysis. Although such association does not necessarily support a causal effect, evidence of an inhibitory role of trans-10,cis-12 CLA on milk fat synthesis has been provided by its postruminal infusion (
Conjugated linoleic acid-induced milk fat depression in lactating ewes is accompanied by reduced expression of mammary genes involved in lipid synthesis.
Diet-induced milk fat depression in dairy cows results in increased trans-10,cis-12 CLA in milk fat and coordinate suppression of mRNA abundance for mammary enzymes involved in milk fat synthesis.
Conjugated linoleic acid-induced milk fat depression in lactating ewes is accompanied by reduced expression of mammary genes involved in lipid synthesis.
Trans-10,cis-12 conjugated linoleic acid alters lipid metabolism of goat mammary epithelial cells by regulation of de novo synthesis and the AMPK signaling pathway.
, diet-induced MFD in cows occurs when the milk fat proportion of trans-10,cis-12 CLA is very low (≤0.16 g/100 g of FA; Table 1, Figure 5A and E). In marine lipid-induced MFD, most often no change in trans-10,cis-12 CLA concentration is observed (
Diets supplemented with starch and corn oil, marine algae, or hydrogenated palm oil differentially modulate milk fat secretion and composition in cows and goats: A comparative study.
). Furthermore, regression analysis, based on 23 studies (Figure 5A, C, and E), reveals that the milk fat proportion of trans-10,cis-12 CLA explained only 27 and 29% of the variation in milk fat content and yield, respectively. Similarly, a recent meta-analysis downplayed the role of this CLA isomer in explaining marine lipid-induced MFD in ovine (
). Overall, this suggests that other biohydrogenation intermediates might also exert antilipogenic effects, or that other factors and mechanisms are involved in the regulation of milk fat synthesis. However, it should be noted here that the very low trans-10,cis-12 CLA concentrations observed in milk fat complicate regression analysis, and the results observed in Figure 5 (A, C, and E) should be interpreted with caution.
Table 1Minimum, maximum, and mean milk fat yield or content, or milk fat proportion of biohydrogenation intermediates associated with milk fat depression,
Data derived from 34 studies (Bhandari et al., 2008; Boeckaert et al., 2008; Enjalbert et al., 2008; Gozho and Mutsvangwa, 2008; Hristov et al., 2009; Iqbal et al., 2009; Longuski et al., 2009; Oelker et al., 2009; Agle et al., 2010; Côrtes et al., 2010; Zhang et al., 2010; Dschaak et al., 2011; Hristov et al., 2011a,b; Martel et al., 2011; Mathew et al., 2011; Benchaar et al., 2012, 2015; He et al., 2012; Brask et al., 2013; Hassanat et al., 2013; Rico and Harvatine, 2013; Boerman et al., 2014; Cruywagen et al., 2015; Kairenius et al., 2015; Pirondini et al., 2015; Rico et al., 2015; Toral et al., 2015; Van Gastelen et al., 2015; Ramirez Ramirez et al., 2016a,b; Szczechowiak et al., 2016; Lopes et al., 2017; Rico et al., 2017).
as well as results of abomasal infusion studies of those intermediates
Effect of lauric acid and coconut oil on ruminal fermentation, digestion, ammonia losses from manure, and milk fatty acid composition in lactating cows.
Interaction of molasses and monensin in alfalfa hay- or corn silage-based diets on rumen fermentation, total tract digestibility, and milk production by Holstein cows.
Effects of partially replacing barley silage or barley grain with dried distillers grains with solubles on rumen fermentation and milk production of lactating dairy cows.
Effect of replacing solvent-extracted canola meal with high-oil traditional canola, high-oleic acid canola, or high-erucic acid rapeseed meals on rumen fermentation, digestibility, milk production, and milk fatty acid composition in lactating dairy cows.
Supplementation of increasing amounts of linseed oil to dairy cows fed total mixed rations: Effects on digestion, ruminal fermentation characteristics, protozoal populations, and milk fatty acid composition.
Linseed oil supplementation to dairy cows fed diets based on red clover silage or corn silage: Effects on methane production, rumen fermentation, nutrient digestibility, N balance, and milk production.
Effect of dietary fat blend enriched in oleic or linoleic acid and monensin supplementation on dairy cattle performance, milk fatty acid profiles, and milk fat depression.
Replacing alfalfa silage with corn silage in dairy cow diets: Effects on enteric methane production, ruminal fermentation, digestion, N balance, and milk production.
Induction of and recovery from milk fat depression occurs progressively in dairy cows switched between diets that differ in fiber and oil concentration.
The effect of buffering dairy cow diets with limestone, calcareous marine algae, or sodium bicarbonate on ruminal pH profiles, production responses, and rumen fermentation.
Effect of dietary starch concentration and fish oil supplementation on milk yield and composition, diet digestibility, and methane emissions in lactating dairy cows.
Reduced-fat dried distillers grains with solubles reduces the risk for milk fat depression and supports milk production and ruminal fermentation in dairy cows.
Short communication: Forage particle size and fat intake affect rumen passage, the fatty acid profile of milk, and milk fat production in dairy cows consuming dried distillers grains with solubles.
Rumen fermentation, methane concentration and fatty acid proportion in the rumen and milk of dairy cows fed condensed tannin and/or fish-soybean oils blend.
Short communication: Effects of lysolecithin on milk fat synthesis and milk fatty acid profile of cows fed diets differing in fiber and unsaturated fatty acid concentration.
Figure 5Relationship between milk fat content (MFC; A–D) or yield (MFY; E–F) and milk fat proportion (g/100 g; FA = fatty acids) of trans-10,cis-12 CLA (A, C, E) or trans-10 18:1 (B, D, F), either (C, D), or not (A, B, E, F), after a natural log-transformation of the milk fat proportion data of trans-10,cis-12 CLA or trans-10 18:1. Square = milk fat content; triangle = milk fat yield; solid line = linear relation with milk fat content; dashed line = linear relation with milk fat yield. The linear relation between the natural log-transformed proportions of both FA and milk fat yield did not result in an improvement of the relation as compared with the non-transformed data (data not shown). Data derived from 23 studies (
Effect of lauric acid and coconut oil on ruminal fermentation, digestion, ammonia losses from manure, and milk fatty acid composition in lactating cows.
Effect of replacing solvent-extracted canola meal with high-oil traditional canola, high-oleic acid canola, or high-erucic acid rapeseed meals on rumen fermentation, digestibility, milk production, and milk fatty acid composition in lactating dairy cows.
Interaction of molasses and monensin in alfalfa hay- or corn silage-based diets on rumen fermentation, total tract digestibility, and milk production by Holstein cows.
Supplementation of increasing amounts of linseed oil to dairy cows fed total mixed rations: Effects on digestion, ruminal fermentation characteristics, protozoal populations, and milk fatty acid composition.
Effect of dietary fat blend enriched in oleic or linoleic acid and monensin supplementation on dairy cattle performance, milk fatty acid profiles, and milk fat depression.
Induction of and recovery from milk fat depression occurs progressively in dairy cows switched between diets that differ in fiber and oil concentration.
Effect of dietary starch concentration and fish oil supplementation on milk yield and composition, diet digestibility, and methane emissions in lactating dairy cows.
Reduced-fat dried distillers grains with solubles reduces the risk for milk fat depression and supports milk production and ruminal fermentation in dairy cows.
Short communication: Forage particle size and fat intake affect rumen passage, the fatty acid profile of milk, and milk fat production in dairy cows consuming dried distillers grains with solubles.
Rumen fermentation, methane concentration and fatty acid proportion in the rumen and milk of dairy cows fed condensed tannin and/or fish-soybean oils blend.
Short communication: Effects of lysolecithin on milk fat synthesis and milk fatty acid profile of cows fed diets differing in fiber and unsaturated fatty acid concentration.
indicated that diets causing lower milk fat concentration and yield are consistently associated with an increase in the milk fat trans-10 18:1 proportion, which has been confirmed by regression analysis of studies with dairy cows (Figure 5B, D, and F) and canonical discriminant analysis (
split data of dairy ewes into a subset with and without MFD. Similar shifts in trans-10 18:1 were observed in both subsets, excluding a major role of this FA in diet-induced MFD in this species. Hence, the potential role of this isomer in diet-induced MFD is equivocal.
Direct evidence of the potential role of this isomer can be provided by postruminal infusion studies or in vitro assessments with cell lines. Downregulated expression of FASN, SCD, and SREBF1 upon incubation of mammary epithelial cells with trans-10 18:1 (
Peroxisome proliferator-activated receptor-γ activation and long-chain fatty acids alter lipogenic gene networks in bovine mammary epithelial cells to various extents.
). In that study, abomasal infusion of 42.6 g of pure trans-10 18:1/d for 4 d increased the milk fat trans-10 18:1 concentration from 0.47 to 1.11 g/100 of g of FA, but no decrease in milk fat secretion was observed. This lack of effect on milk fat content or yield was interpreted as strong evidence that trans-10 18:1 does not inhibit milk fat synthesis during MFD. However, the average transfer efficiency of the abomasally infused trans-10 18:1 into milk fat was only 15% (
reported a mean transfer efficiency from the abomasum into milk fat of 32.1% for this intermediate. Furthermore, the mean milk fat proportion of trans-10 18:1 is higher (1.91 g/100 of g of FA; Table 1) than the proportion obtained by
upon abomasal infusion (1.11 g/100 g of FA). As such, the difference in milk fat proportion of trans-10 18:1 between the control and the trans-10 18:1 infusion might have been too small to induce significant changes between both treatments (expected decrease of 0.16 g of milk fat per 100 g of milk, based on the equation presented in Figure 5B). Indeed, a higher milk fat trans-10 18:1 proportion (4.37 g/100 g of FA) upon abomasal infusion decreased the milk fat content and yield by 21.3 and 19.5%, respectively, in the study by
. Nevertheless, in that study, a mixture of 18:1 FA methyl esters was used, containing (g/100 g of FA) cis-9 18:1 (9.45), cis-12 18:1 (3.35), trans-10 18:1 (37.3), trans-11 18:1 (37.4), and trans-12 18:1 (2.66) as major isomers. As such, MFD could not be directly attributed to trans-10 18:1. To our knowledge, no other abomasal infusion studies using relatively pure trans-10 18:1 were performed. This gap in the literature also concerns small ruminants, for which high milk trans-10 18:1 concentrations have been reported in the absence of clear MFD (
Effect of extruded linseeds alone or in combination with fish oil on intake, milk production, plasma metabolite concentrations and milk fatty acid composition in lactating goats.
highlighted trans-10 18:1 to be consistently associated with reduced concentrations and yields of de novo synthesized milk FA. However, only in part of the studies this resulted in an overall MFD. Indeed, in cases without MFD, the decreased secretion of de novo synthesized FA seemed counteracted by increments of preformed FA.
suggested that cis-10,trans-12 CLA has antilipogenic effects based on abomasal infusions of geometric isomers of 10, 12 CLA. However, in that study, cis-10,trans-12 CLA was infused in combination with trans-10,cis-12 CLA, which is known to have an antilipogenic effect (
Diet-induced milk fat depression in dairy cows results in increased trans-10,cis-12 CLA in milk fat and coordinate suppression of mRNA abundance for mammary enzymes involved in milk fat synthesis.
). Nevertheless, abomasal infusion of 4.137 g of trans-10,cis-12 CLA/d resulted in a similar milk fat decrease as compared with a combination of 1.802 g of trans-10,cis-12 CLA and 1.194 g of cis-10,trans-12 CLA/d, indicating a potential role of the latter FA isomer in MFD. No other studies showing a possible direct effect of cis-10,trans-12 CLA on milk fat synthesis have been performed since 2005. Furthermore, recent studies did not report the milk fat proportion of this CLA isomer (Table 1), potentially indicating that cis-10,trans-12 CLA is hardly observed in milk fat of dairy cows and is not a major cause of diet-induced MFD.
Trans-9,cis-11 CLA
The potential role of trans-9,cis-11 CLA in MFD was shown by
, who abomasally infused 5 g of trans-9,cis-11 CLA/d and reduced both the milk fat content and yield by 15%. Nevertheless, in that study, the milk fat proportion of trans-9,cis-11 CLA was 0.38 g/100 g of FA, which is much higher than the maximum proportion of 0.10 g/100 g of FA presented in Table 1. It is not clear whether milk fat proportions of trans-9,cis-11 CLA below or equal to 0.10 g/100 g of FA would also reduce milk fat synthesis.
Other FA
An in vitro study using 13C-labeled 18:3n-3 and rumen inoculum from sheep speculated on the potential contribution of 18:3 isomers (of which some were unidentified) in marine lipid-induced MFD (
investigated the effect of intravenous infusion of cis-9,trans-11,cis-15 18:3 and cis-9,trans-13,cis-15 18:3 on milk fat synthesis in lactating dairy cows. However, their study offered no support for a role of those isomers in MFD, although this does not exclude the potential involvement of other 18:3 isomers.
Studies conducted in cows, ewes, and does have shown that MFD accompanied increases in milk fat or omasal digesta proportions of other 18-carbon FA, such as cis-11 18:1, trans-4 to trans-9 18:1, trans-8,trans-10 CLA, trans-10,trans-12 CLA, trans-10,cis-15 18:2, and 10-oxo-18:0 (
Diet-induced milk fat depression is associated with alterations in ruminal biohydrogenation pathways and formation of novel fatty acid intermediates in lactating cows.
). Their origin is likely different and would not always be associated with biohydrogenation. For example, the increased milk fat proportion of cis-11 18:1 under fish oil-induced MFD conditions (
) might result from its supply of marine lipids and the concomitant inhibition of 18:1 saturation, rather than from an increased production in the rumen through C18 biohydrogenation. This hypothesis is supported by the in vitro incubation of 13C-labeled UFA with rumen inoculum from cows (
). As such, PUFA originating directly from fish oil might contribute, at least in part, to MFD. Indeed, abomasal infusion of 406 g of fish oil/d resulted in a modest decrease in milk fat content and yield (12 and 17%, respectively) in the experiment of
Effects of abomasal infusion of conjugated linoleic acids, Sterculia foetida oil, and fish oil on production performance and the extent of fatty acid Δ9-desaturation in dairy cows.
Effects of ruminal or duodenal supply of fish oil on milk fat secretion and profiles of trans-fatty acids and conjugated linoleic acid isomers in dairy cows fed maize silage.
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