Next Article in Journal
Infection of Mammary Glands of Small Mammals in Eastern North America by Helminths
Previous Article in Journal
Effects of Receiving Two Initial Feedings of Colostrum on the Average Daily Gain and Health of Pre-Weaning Group Housed Holstein Heifer Calves
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Animals
Volume 11
Issue 11
10.3390/ani11113210
animals-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Milk Odd and Branched Chain Fatty Acids in Dairy Cows: A Review on Dietary Factors and Its Consequences on Human Health

by
Sidi Ka Amar Abdoul-Aziz
,
Yangdong Zhang
and
Jiaqi Wang
*
State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, No. 2 Yuanmingyuan West Road, Beijing 100193, China
*
Author to whom correspondence should be addressed.
Animals 2021, 11(11), 3210; https://doi.org/10.3390/ani11113210
Submission received: 28 September 2021 / Revised: 1 November 2021 / Accepted: 2 November 2021 / Published: 10 November 2021
(This article belongs to the Section Cattle)
Browse Figure
Versions Notes

Abstract

:

Simple Summary

The objective of this review is to highlight the importance of odd and branched chain fatty acids and dietary factors that may affect their content in milk acids in dairy cows. The primary source of odd and branched chain fatty acids is ruminal bacteria. In contrast to saturated fatty acids, odd and branched chain fatty acids have health protective effects against certain diseases as cardiovascular diseases, type II diabetes, cancers, Alzheimer’s disease and metabolic syndrome. Ruminant products are the main source of these fatty acids in the human diet. Odd and branched chain fatty acids profile in cow milk is mainly affected by dietary fatty acids and fatty acids metabolism in the rumen. Additionally, lipid mobilization in the body and fatty acids metabolism in mammary glands affect the milk odd and branched chain fatty acids profile. Understanding the origin of odd and branched chain fatty acids in milk and manipulating the diet of dairy cows to produce odd and branched chain fatty acids-enriched milk can be of scientific and industrial significance.

Abstract

This review highlights the importance of odd and branched chain fatty acids (OBCFAs) and dietary factors that may affect the content of milk OBCFAs in dairy cows. Historically, OBCFAs in cow milk had little significance due to their low concentrations compared to other milk fatty acids (FAs). The primary source of OBCFAs is ruminal bacteria. In general, FAs and OBCFAs profile in milk is mainly affected by dietary FAs and FAs metabolism in the rumen. Additionally, lipid mobilization in the body and FAs metabolism in mammary glands affect the milk OBCFAs profile. In cows, supplementation with fat rich in linoleic acid and α-linolenic acid decrease milk OBCFAs content, whereas supplementation with marine algae or fish oil increase milk OBCFAs content. Feeding more forage rather than concentrate increases the yield of some OBCFAs in milk. A high grass silage rate in the diet may increase milk total OBCFAs. In contrast to saturated FAs, OBCFAs have beneficial effects on cardiovascular diseases and type II diabetes. Furthermore, OBCFAs may have anti-cancer properties and prevent Alzheimer’s disease and metabolic syndrome.
Keywords:
milk; odd; branched; fatty; acids; cows; dietary

1. Introduction

The main lipids in milk are fatty acids (FAs), acylglycerols, and cholesterol [1]. Milk fat contains a small quantity of odd and branched chain fatty acids (OBCFAs). However, OBCFAs appear to be differentially accumulated in adipose tissue and milk of cows [2], goats [3], and sheep [4]. The content of these FAs in milk originated from metabolites synthesized by ruminal bacterial, with a large variation in their FAs profiles [5]. Amylolytic bacteria produce more linear odd chain and anteiso FAs than iso FAs, whereas cellulolytic bacteria produce more iso FAs [6]. The biosynthesis of OBCFAs in the rumen is the primary source of milk from ruminant animals [7]. The characteristic of FAs in the ruminal bacteria is largely composed by OBCFAs in the membrane lipids (C15:0; anteiso C15:0; iso C15:0; C17:0; iso C17:0; C17:1 and anteiso C17:0) [8].
OBCFAs have been used as a marker of ruminal bacterial colonization following consuming of fresh herbs [9,10]. Furthermore, some studies have shown that OBCFAs could be used as markers for quantifying ruminal bacteria [11]. Linear odd chain FAs (C15:0 and C17:0) have been used as biomarkers to identify the link between dairy product consumption and disease outcomes [12,13].
Milk contains essential nutrients that are beneficial to human health, e.g., liposoluble vitamins, carotenoids, calcium, bioactive peptides, essential FAs, and sphingolipids [14]. However, cholesterol, saturated FAs, and trans FAs have been associated with increased risk of type II diabetes, obesity, and cardiovascular diseases, which has prompted health authorities to recommend a low consumption of dairy products. As a result, the consumption of OBCFAs is low [15]. Nevertheless, there is an increasing interest of milk OBCFAs, following research reported that several OBCFAs have potential health benefits in humans [16,17]. Recently, it has been reported that during early life Branched-chain fatty acids (BCFAs) play a role in human gut health [18].
OBCFAs are present in small quantities in several vegetables that are incorporated in feedstuff [19]. Some studies have reported that <100 g of OBCFAs per kg of milk can be obtained from feeding, even though all dietary OBCFAs are transferred into milk [20]. This review discusses the importance and origin of milk OBCFAs and the dietary factors that affect OBCFAs biosynthesis in dairy cows.

2. Origin of Milk OBCFAs in Dairy Cows

Decades ago, OCFAs had little significance due to their low physiological concentrations compared to non-OCFAs [21]. In the human body, a large part of OCFAs undergo β-oxidation [22]. While the β-oxidation of OCFAs results in propionyl-CoA, the β-oxidation of even-chain FAs results in cetyl-CoA [17]. Studies have reported that OCFAs formation may occur in the human body via α-oxidation [23]. Furthermore, propionate derived from intestinal bacteria can be used to produce OCFAs in the liver [24].
Milk fat contains a small quantity of OBCFAs. The major OBCFAs in milk are C15:0, C17:0, iso C13:0, iso C14:0, iso C15:0, iso C16:0, iso C17:0, anteiso C15:0, and anteiso-C17:0 [25]. Most of these OBCFAs originate from ruminal bacteria [7]. However, the profile of OBCFAs in milk does not closely match the profile of OBCFAs in ruminal bacteria. The difference between these profiles suggests that a small amount of OBCFAs may originate from post ruminal synthesis [26].
The profile of OBCFAs in ruminal bacteria is primarily determined through the enzymes that catalyze FAs’ synthesis in microorganisms, rather than the availability of the precursors [27]. As a result, iso-FAs are abundant in the solid phase of cellulolytic bacteria, while anteiso C15:0 is abundant in the liquid phase of bacteria involved in sugar and pectin fermentation [28]. Bacterial membrane lipids are the main source of OBCFAs in the rumen [29]. In bacteria, de novo synthesis of OBCFAs can proceed systematically. OCFAs can be synthesized via the valerate or propionate elongation pathways [6], with propionyl-CoA rather of acetyl-CoA as the precursor [8]. In addition, contents of OCFAs are higher in milk than in plasma [30], indicating that some OCFAs and anteiso FAs are produced in mammary glands [31]. Even though de novo synthesis of linear OCFAs in mammary glands are not significant in milk [32], several studies have reported that some linear OCFAs such as C15:0 and C17:0 are synthesized from propionate in mammary glands and adipose tissue [33,34]. Propionyl-CoA can serve as the precursor for the synthesis of OCFAs [35]. Precursors of BCFAs are valine, leucine, and isoleucine, which are branched chain amino acids such as 2-methyl butyric, isobutyric, and isovaleric acids [6]. Propionate may be indirectly used in the synthesis of some BCFAs by incorporating methylmalonyl-CoA into the carboxylation product [36]. As a result, a single change in the production of BCFAs or linear-chain FAs is at the specific precursor or product level [8].
When cows are supplemented with calcium soap and mixed animal/vegetable fats, 70% of dietary FAs are recovered in the small intestine, of which 106 g/d is derived from the rumen regardless of diet. These FAs are largely OBCFAs, and more than 90% of FA with <14 carbons disappear [37]. Some FAs that are not present in the diet appear in the duodenal digesta, and they are either branched (e.g., C15:0 and C16:0) or odd-numbered carbon chains (C15:0 and C17:0); therefore, they are unique to the ruminal bacteria [38].
Milk OBCFAs may originate from (1) ruminal bacteria that produce OBCFAs, which are subsequently transferred to milk or (2) de novo synthesis in mammary glands.
Figure 1 provides an illustration of the origin of milk OBCFAs in dairy cows.

3. Dietary Factors Influencing Milk OBCFAs

The nutritional quality of feed influences milk yield and quality in dairy cows [39]. The profile of milk FAs is largely affected by dietary lipid composition and FAs metabolism in rumen [40,41] and mammary glands [42].
Seed, vegetable, and fish oils contribute to an optimal milk composition [43,44]. When cows are fed linseed or flaxseed oil, the ruminal biohydrogenation of cis-9, cis-12, cis-15 C18:3 generates a high amount of FAs isomers [45]. For example, dietary supplements containing flaxseed increase the content of C18:0, C18:1 9c, C18:1 9t, and C18:2 9c 12c in the rumen without significant changes in the content of cis-9, cis-12, cis-15 18:3 and induce the disappearance of the corresponding OCFAs and anteiso FAs [46]. In lactating cows, ground linseed does not affect milk yield or composition, but increases n-3 FAs and decreases OCFAs with ≤16 carbons [47]. The quantity of ground flaxseed in the supplement is negatively associated with OBCFAs in milk and butyrate and acetate in the rumen and positively associated with propionate in the rumen [48]. Dietary FAs composition may affect FAs metabolism in the rumen. Supplementing fat rich in saturated FAs increases the content of (Saturated Fatty Acids) SFAs in milk [49].
Even though they affect ruminal microbial growth and reduce de novo synthesis of microbial FAs, dietary lipids increase FAs uptake in mammary glands [50,51]. Dietary lipids affect the uptake of individual FAs by ruminal bacteria, resulting in a reduction in FAs de novo synthesis by bacteria, which alters the profile of milk FAs [52]. In addition, lipids may inhibit lipogenesis in the mammary glands, likely mediated via the (Conjugated linoleic acids) CLA isomer 18:2 tans 10, cis-12 that is synthesized in the rumen [53].
Derived metabolites of volatile FAs (VFAs), such as butyrate, propionate, and acetate, may be used for FAs de novo synthesis by ruminal bacteria. Therefore, these primary end products of ruminal fermentation can affect FAs metabolism in the rumen and mammary glands. Infusing propionate into the rumen increases concentrations of propionate in blood and C15:0 and C17:0 in milk, but not in the rumen [54]. According to Bauman et al. [50] milk C17:0 and cis-9 C17:1 concentrations and acetate-to-propionate ratios are not associated with propionate concentrations in the rumen due to the presence of C17:0 and cis-9 C17:1 in the diet. Fievez et al. [5] reported that there is a positive association between iso FAs and linear OCFAs in milk and acetate and propionate in the rumen. The authors observed that some OBCFAs in milk were associated with the enrichment and relative activities of ruminal bacteria that synthesize OBCFAs. This means that OCFAs content in milk may provide information on specific ruminal conditions [25]. Therefore, the profile of milk OBCFAs might be used as a potential non-invasive method to reveal characteristics of ruminal function [5]. According to Cívico et al. [55] OBCFAs from dairy goats are associated with dietary composition of FAs and may be explored as potential biomarkers in the rumen fermentation. Due to the post-ruminal modifications of OBCFAs, caution should be exercised when using milk OBCFAs to assess ruminal VFAs [26].
Even though yield of C15:0, C17:0, iso C15:0, iso C17:0, anteiso-C15:0, and anteiso-C17:0 in milk is related to their duodenal content [56], yield is higher in milk than in the duodenum [20].
The modification of milk BCFAs by manipulating dietary fats is not conclusive [50,51,52,53,54,55,56,57]. In general, fat supplementation affects ruminal microbial populations [58] and FAs in milk [50]. For example, addition of unsaturated FAs to the diet reduces saturated FAs in bovine milk, whereas increased unsaturated FAs in dairy cow milk and increased concentrations of dietary 18:3n-3 and 18:2n-6 could effectively increase milk content of cis-9, trans-11 CLA in dairy cow [59,60,61,62,63] while lowering OBCFAs proportions in milk [25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64]. In contrast, fish oil or microalgae supplementation increases milk OBCFAs concentrations in dairy cows [65,66]. Infusion of branched chain VFAs in the rumen did not affect linear odd-chain FAs, odd anteiso FAs or odd iso FAs in ruminal liquid, ruminal solid, or milk fat. Nevertheless, milk OBCFAs, particularly C13:0, iso C15:0, C17:1 and iso C17:0, varied slightly [54].
The type of dietary fat may affect the FAs profile in milk. Substitution of fat abundant in C16:0 FAs with fat abundant in C18:2n-6 FAs at 30 g/kg of DM (Dry Matter) feed in low forage diet reduced the yield of anteiso 13:0 FAs and anteiso 15:0 FAs in milk; however, mixing both types of fat at equal proportions (each at 15 g/kg of DM feed) increased C14:0 iso and C16:0 iso FAs yield in milk [16]. In addition, long-chain PUFAs (Polyunsaturated fatty acids), such as cis-9, cis-12 C18:2, have a toxic effect on ruminal cellulolytic bacteria [67]. Replacing prilled palm fat with sunflower oil linearly reduced the concentration and yield of C13:0 anteiso with non-significant effects on the yield of C15:0 anteiso and total anteiso FAs in milk [16]. These results are probably attributed to the reduction of amylolytic bacteria in the rumen, which are enriched with anteiso FAs according to [5]. Therefore, supplementation with PUFAs may reduce the amount of milk FAs of bacterial origin.
Dietary type and green feeds influence FAs in milk. In grass silage diet, inclusion of vegetable oils abundant in 18:2n-6 decreased the proportions of numerous iso and anteiso FAs in milk [68]. However, those results were not observed when corn silage and grass silage were mixed in the diet [69]. BCFAs, particularly iso FAs in milk, can be enriched by increasing dietary forage in the diet [16,60,70]. Increasing high-quality grass silage in the diet from 50% to 85% resulted in an increase in linear OCFAs, iso C15:0, and total OBCFAs in milk [70]. A substitution of grass silage with corn silage in the diet increases starch and reduces neutral detergent fiber (NDF), resulting in changes in ruminal pH, microbial populations, VFAs production [71,72], and possibly FAs in the rumen. Patel et al. [70] demonstrated that milk OBCFAs are positively associated with NDF amount in the diet. Morales-Almaráz et al. [73] reported that forage and pasture in the diet increase FAs content in milk. However, an increase in dietary concentrate reduces the efficiency of transit of iso- and anteiso- C15:0 from the duodenal digest to milk. Replacing wheat with corn in the diet reduces bacterial BCFAs content and even-chain saturated FAs in the rumen [46]. According to Bougouin et al. [74] diets containing starch from wheat and maize grain increases milk concentration of various OBCFAs (e.g., C5:0, C7:0, iso C15:0, anteiso C15:0, and anteiso C17:0) to a greater extent than diets containing saturated FAs, extruded rapeseeds, and extruded sunflower seeds. The red clover silage incorporation in dairy cows’ diets increases the amounts of OBCFAs in milk fat [75]. Therefore, OBCFAs in the rumen and milk can be affected by the amount and type of lipids in the diet, forage-to-concentrate ratio, and forage type and proportion in the diet (Table 1, Table 2 and Table 3).

4. Milk OBCFAs and Human Health

Ruminant products are the main source of OBCFAs in the human diet. OBCFAs are produced by ruminal bacteria [8]. The first scientific findings on the negative effects of animal fats on human health generated considerable interest on the chemical composition of these fats. Additionally, it prompted health authorities to recommend a low consumption of dairy products [83].
More than 150 different diseases are associated with high dietary lipids, including type II diabetes [84,85], high blood pressure and artery plaque formation [86], obesity [87], neurological disturbances [88], and certain cancers [89,90]. There is a positive association between dairy fat consumption and plasma saturated FAs; therefore, high consumption of dairy fat might be associated with increased risk of cardiovascular diseases. Further studies have shown that these are the ECFAs (Even Chain Fatty Acids) which are related to type 2 diabetes, inflammation and heart disease [91,92,93]. However, Kim and Je [94] reported that dairy intake was negatively correlated with metabolic syndrome, and numerous research showed that there is an association between higher dietary consumption of full-fat dairy and lessen the incidence of cardiovascular disease and type 2 diabetes [95,96,97]. Even though, some previous studies oppose this hypothesis [98].
There is not enough evidence on the link between odd chain FAs (OCFAs) and heart disease and metabolic syndrome. The evidence suggests that OCFAs might have protective effects. Yu and Hu [99] reported a non-significant correlation between C15:0 consumption and heart disease and metabolic disorders. Similar results have been reported by Yakoob et al. [100] and Santaren et al. [101]. The evidence shows non-significant inverse associations OCFAs consumption and atherosclerosis [102,103] and between C15:0 and C17:0 consumption and diabetes [99]. The intake of C15:0 as an active fatty acid diet reduced in vivo anemia, inflammation, fibrosis and dyslipidemia, by mending the function of mitochondria [104]. OCFAs in diet were related to decrease the risk of chronic inflammation, adiposity, cardiovascular disease, type 2 diabetes, metabolic syndrome, nonalcoholic steatohepatitis (NASH), pancreatic cancer and chronic obstructive pulmonary disease in human [91,92,93,94,95,96,97,98,99,100,101,102,103,104,105,106,107,108,109,110,111,112,113]. A meta-analysis of 29 studies discussed the protective effects of OCFAs and of very-long even chain saturated FAs on type II diabetes [106]. OCFAs (C15:0 and C17:0) are significantly and inversely correlated with arterial stiffness and may be negatively correlated with atherosclerosis [114,115]. Tissue levels of OCFAs are lower in patients with Alzheimer’s than in healthy controls [116]. Furthermore, OCFAs might have anti-carcinogenic properties [6]. There are inverse associations between OCFAs consumption and prediabetes and type II diabetes [117,118], cardiovascular disease [119], and insulin resistance [120]. OCFAs increase biotin levels in deficient cases [121] and in cases of peroxisomal disorders [122] and improves cell membrane fluidity [123]. In addition, OCFAs may be used in the treatment of disorders linked to propionate, methylmalonic, and biotin [124].
More than 4% of the total FAs in milk are branched chain FAs (BCFAs) [6]. Dairy and meat from ruminants are the main sources of BCFAs [125]. The importance of BCFAs is attributed to its anticancer activity [6], including on breast cancer cells [126]. Iso C15 has anti-tumor effects on lymphomatoid tumors [66], decreases intestinal necrosis in neonates [127], plays a role in cancer cell death [128], and enhances pancreatic β-cell function [129]. In addition, BCFAs prevent FAs synthesis in tumor cells [130], which rely more on FAs biosynthesis than healthy cells [131].
The recent evidence of large and well-controlled research, meta-analyses and reviews showed that dairy full-fat do not increase cardiometabolic disease risk and may have protective effect against type 2 diabetes and cardiovascular disease [132,133].

5. Conclusions

The milk profile of OBCFAs is affected by dietary FAs intake, FAs metabolism in the rumen and mammary glands, and lipid mobilization in the body. Forage and silage in dairy cows’ diets are important in an increasing the amounts of milk OBCFAs. Ruminant products are the main source of OBCFAs in the human diet. OBCFAs have a protective effect on diabetes, Alzheimer’s disease, certain cancers, cardiovascular disease, and atherosclerosis. Understanding the origin of OBCFAs in milk and manipulating the diet of dairy cows to produce OBCFAs-enriched milk can be of scientific and industrial significance.

Author Contributions

Conceptualization, J.W.; Writing-review and editing, S.K.A.A.-A.; Project administration, Y.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by the Beijing Milk Research Team, the Key Laboratory of Quality and Safety Control for Dairy Products, the Ministry of Agriculture and Rural Affairs of Chinese Academy of Agricultural Sciences, the Agricultural Science and Technology Innovation Program (ASTIP-IAS12), the Modern Agro-Industry Technology Research System of the PR China (CARS-36), and the Scientific Research Project for Major Achievements of the Agricultural Science and Technology Innovation Program (CAAS-ZDXT2019004).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Acknowledgments

Special thanks go to Jiaqi Wang and Yangdong Zhang, Chinese Academy of Agricultural Sciences, Institute of Animal Science, for their participation in the smooth running of this study. Huang Guoxin, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, for the Skillful technical assistance. The help of the Milk Research Teamis is also highly appreciated.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Bainbridge, M.L.; Cersosimo, L.M.; Wright, A.D.G.; Kraft, J. Content and composition of branched-chain fatty acids in bovine milk are affected by lactation stage and breed of dairy cow. PLoS ONE 2016, 11, e0150386. [Google Scholar] [CrossRef] [Green Version]
  2. Polidori, P.; Maggi, G.L.; Moretti, V.M.; Valfre, F.; Navarotto, P.A. Note on the effect of use of bovine somatotropin on the fatty acid composition of the milk fat in dairy cows. Anim. Sci. 1993, 57, 319–322. [Google Scholar] [CrossRef]
  3. Rojas, A.; López-Bote, C.; Rota, A.; Martin, L.; Rodriguez, P.L.; Tovar, J.J. Fatty acid composition of Verata goat kids fed either goat milk or commercial milk replacer. Small Rumin. Res. 1994, 14, 61–66. [Google Scholar] [CrossRef]
  4. Jenkins, T.C. Butylsoyamide protects soybean oil from ruminal biohydrogenation: Effects of butylsoyamide on plasma fatty acids and nutrient digestion in sheep. J. Anim. Sci. 1995, 73, 818–823. [Google Scholar] [CrossRef] [PubMed]
  5. Fievez, V.; Colman, E.; Stefanov, I.; Vlaeminck, B. Milk odd- and branched-chain fatty acids as biomarkers of rumen function—An update. Anim. Feed Sci. Technol. 2012, 172, 51–65. [Google Scholar] [CrossRef]
  6. Vlaeminck, B.; Fievez, V.; Cabrita, A.R.J.; Fonseca, A.J.M.; Dewhurst, R.J. Factors affecting odd-and branched-chain fatty acids in milk: A review. Anim. Feed Sci. Technol. 2006, 131, 389–417. [Google Scholar] [CrossRef]
  7. Keeney, M.; Katz, I.; Allison, M.J. On the probable origin of some milk fat acids in rumen microbial lipids. J. Am. Oil Chem. Soc. 1962, 39, 198–201. [Google Scholar] [CrossRef]
  8. Kaneda, T. Iso-and anteiso-fatty acids in bacteria: Biosynthesis, function, and taxonomic significance. Microbiol. Mol. Biol. Rev. 1991, 55, 288–302. [Google Scholar] [CrossRef] [Green Version]
  9. Kim, E.J.; Sanderson, R.; Dhanoa, M.S.; Dewhurst, R.J. Fatty acid profiles associated with microbial colonization of freshly ingested grass and rumen biohydrogenation. Int. J. Dairy Sci. 2005, 88, 3220–3230. [Google Scholar] [CrossRef] [Green Version]
  10. Liu, K.; Hao, X.; Li, Y.; Luo, G.; Zhang, Y.; Xin, H. The relationship between odd-and branched-chain fatty acids and microbial nucleic acid bases in rumen. Asian-Australas. J. Anim. Sci. 2017, 30, 1590. [Google Scholar] [CrossRef] [Green Version]
  11. Vlaeminck, B.; Dufour, C.; Van Vuuren, A.M.; Cabrita, A.M.R.; Dewhurst, R.J.; Demeyer, D.; Fievez, V. Potential of odd and branched chain fatty acids as microbial markers: Evaluation in rumen contents and milk. J. Dairy Sci. 2005, 88, 1031–1041. [Google Scholar] [CrossRef] [Green Version]
  12. Warensjö, E.; Jansson, J.-H.; Berglund, L.; Boman, K.; Ahren, B.; Weinehall, L.; Vessby, B. Estimated intake of milk fat is negatively associated with cardiovascular risk factors and does not increase the risk of a first acute myocardial infarction. A prospective case—Control study. Br. J. Nutr. 2004, 91, 635–642. [Google Scholar] [CrossRef] [PubMed]
  13. Wolk, A.; Vessby, B.; Ljung, H.; Barrefors, P. Evaluation of a biological marker of dairy fat intake. Am. J. Clin. Nutr. 1998, 68, 291–295. [Google Scholar] [CrossRef] [PubMed]
  14. Fontecha, J.M.; Rodriguez-Alcala, L.V.; Calvo, M.; Juárez, M. Bioactive milk lipids. Curr. Nutr. Food Sci. 2011, 7, 155–159. [Google Scholar] [CrossRef] [Green Version]
  15. Mills, S.; Ross, R.P.; Hill, C.; Fitzgerald, G.F.; Stanton, C. Milk intelligence: Mining milk for bioactive substances associated with human health. Int. Dairy J. 2011, 21, 377–401. [Google Scholar] [CrossRef]
  16. Vazirigohar, M.; Dehghan-Banadaky, M.; Rezayazdi, K.; Nejati-Javaremi, A.; Mirzaei-Alamouti, H.; Patra, A.K. Short communication: Effects of diets containing supplemental fats on ruminal fermentation and milk odd-and branched-chain fatty acids in dairy cows. J. Dairy Sci. 2018, 101, 6133–6141. [Google Scholar] [CrossRef] [Green Version]
  17. Jenkins, B.; West, J.; Koulman, A. A review of odd-chain fatty acid metabolism and the role of pentadecanoic acid (C15: 0) and heptadecanoic acid (C17: 0) in health and disease. Molecules 2015, 20, 2425–2444. [Google Scholar] [CrossRef] [Green Version]
  18. Xin, H.; Ma, T.; Xu, Y.; Chen, G.; Chen, Y.; Villot, C.; Steele, M.A. Characterization of fecal branched-chain fatty acid profiles and their associations with fecal microbiota in diarrheic and healthy dairy calves. J. Dairy Sci. 2021, 104, 2290–2301. [Google Scholar] [CrossRef] [PubMed]
  19. Diedrich, M.; Henschel, K.-P. The natural occurrence of unusual fatty acids. Part 1. Odd numbered fatty acids. Food/Nahrung. 1990, 34, 935–943. [Google Scholar] [CrossRef]
  20. Dewhurst, R.J.; Moorby, J.M.; Vlaeminck, B.; Fievez, V. Apparent recovery of duodenal odd-and branched-chain fatty acids in milk of dairy cows. J. Dairy Sci. 2007, 90, 1775–1780. [Google Scholar] [CrossRef] [Green Version]
  21. Horning, M.G.; Martin, D.B.; Karmen, A.; Vagelos, P.R. Fatty acid synthesis in adipose tissue. J. Biol. Chem 1961, 236, 669–672. [Google Scholar] [CrossRef]
  22. Eaton, S.; Bartlett, K.B.; Pourfarzam, M. Mammalian mitochondrial β-oxidation. Biochem. J. 1996, 320, 345–357. [Google Scholar] [CrossRef]
  23. Foulon, V.; Sniekers, M.; Huysmans, E.; Asselberghs, S.; Mahieu, V.; Mannaerts, G.P.; Casteels, M. Breakdown of 2-hydroxylated straight chain fatty acids via peroxisomal 2-hydroxyphytanoyl-coa lyase a revised pathway for the $α$-oxidation of straight chain fatty acids. J. Biol. Chem. 2005, 280, 9802–9812. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Weitkunat, K.; Schumann, S.; Nickel, D.; Hornemann, S.; Petzke, K.J.; Schulze, M.B.; Klaus, S. Odd-chain fatty acids as a biomarker for dietary fiber intake: A novel pathway for endogenous production from propionate. Am. J. Clin. Nutr. 2017, 105, 1544–1551. [Google Scholar] [CrossRef] [Green Version]
  25. Fievez, V.; Van Looveren, J.; Wanzele, W.; Vlaeminck, B.; Van Straalen, W.; Wade, K.; Lacroix, R. Knowledge discovery in milk fatty acid databases applied to suboptimal milk production. In Proceedings of the 5th Conference of the European Federation for Information Technology in Agriculture, Food Environment (EFITA), Vila Real, Portugal, 25–28 July 2005; Universidade de Tras-os-Montes e Alto Douro: Vila Real, Portugal, 2005; pp. 1019–1023. [Google Scholar]
  26. Vlaeminck, B.; Gervais, R.; Rahman, M.M.; Gadeyne, F.; Gorniak, M.; Doreau, M.; Fievez, V. Postruminal synthesis modifies the odd-and branched-chain fatty acid profile from the duodenum to milk. J. Dairy Sci. 2015, 98, 4829–4840. [Google Scholar] [CrossRef]
  27. Vlaeminck, B.; Fievez, V.; Demeyer, D.; Dewhurst, R.J. Effect of forage: Concentrate ratio on fatty acid composition of rumen bacteria isolated from ruminal and duodenal digesta. J. Dairy Sci. 2006, 89, 2668–2678. [Google Scholar] [CrossRef]
  28. Bessa, R.J.B.; Maia, M.R.G.; Jerónimo, E.; Belo, A.T.; Cabrita, A.R.J.; Dewhurst, R.J.; Fonseca, A.J.M. Using microbial fatty acids to improve understanding of the contribution of solid associated bacteria to microbial mass in the rumen. Anim. Feed Sci. Technol. 2009, 150, 197–206. [Google Scholar] [CrossRef]
  29. Mackie, R.I.; White, B.A.; Bryant, M.P. Lipid metabolism in anaerobic ecosystems. Crit. Rev. Microbiol. 1991, 17, 449–479. [Google Scholar] [CrossRef]
  30. Kay, J.K.; Weber, W.J.; Moore, C.E.; Bauman, D.E.; Hansen, L.B.; Chester-Jones, H.; Crooker, B.A.; Baumgard, L.H. Effects of week of lactation and genetic selection for milk yield on milk fatty acid composition in Holstein cows. J. Dairy Sci. 2005, 88, 3886–3893. [Google Scholar] [CrossRef] [Green Version]
  31. Smith, S. The animal fatty acid synthase: One gene, one polypeptide, seven enzymes. FASEB J. 1994, 8, 1248–1259. [Google Scholar] [CrossRef]
  32. Croom, W.J., Jr.; Bauman, D.E.; Davis, C.L. Methylmalonic acid in low-fat milk syndrome. J. Dairy Sci. 1981, 64, 649–654. [Google Scholar] [CrossRef]
  33. Dodds, P.F.; Guzman, M.G.; Chalberg, S.C.; Anderson, G.J.; Kumar, S. Acetoacetyl-CoA reductase activity of lactating bovine mammary fatty acid synthase. J. Biol. Chem. 1981, 256, 6282–6290. [Google Scholar] [CrossRef]
  34. Massart-Leën, A.M.; Roets, E.; Peeters, G.; Verbeke, R. Propionate for fatty acid synthesis by the mammary gland of the lactating goat. J. Dairy Sci. 1983, 66, 1445–1454. [Google Scholar] [CrossRef]
  35. Crown, S.B.; Marze, N.; Antoniewicz, M.R. Catabolism of Branched Chain Amino Acids Contributes Significantly to Synthesis of Odd- Chain and Even-Chain Fatty Acids in 3T3-L1 Adipocytes. PLoS ONE 2015, 10, e0145850. [Google Scholar] [CrossRef] [Green Version]
  36. Vlaeminck, B.; Fievez, V.; Tamminga, S.; Dewhurst, R.J.; Van Vuuren, A.; De Brabander, D.; Demeyer, D. Milk Odd- and Branched-Chain Fatty Acids in Relation to the Rumen Fermentation Pattern. J. Dairy Sci. 2006, 89, 3954–3964. [Google Scholar] [CrossRef] [Green Version]
  37. Wu, Z.; Ohajuruka, O.A.; Palmquist, D.L. Ruminal synthesis, biohydrogenation, and digestibility of fatty acids by dairy cows. J. Dairy Sci. 1991, 74, 3025–3034. [Google Scholar] [CrossRef]
  38. Noble, R.C. Digestion, absorption and transport of lipids in ruminant animals. Lipid. Met. Rumin. Anim. 1981, 2, 57–93. [Google Scholar]
  39. Huhtanen, P.; Rinne, M.; Mäntysaari, P.; Nousiainen, J. Integration of the effects of animal and dietary factors on total dry matter intake of dairy cows fed silage-based diets. Animal 2011, 5, 691–702. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  40. Jenkins, T.C.; Wallace, R.J.; Moate, P.J.; Mosley, E.E. Board-invited review: Recent advances in biohydrogenation of unsaturated fatty acids within the rumen microbial ecosystem. J. Anim. Sci. 2008, 86, 397–412. [Google Scholar] [CrossRef]
  41. Lock, A.L.; Bauman, D.E. Modifying milk fat composition of dairy cows to enhance fatty acids beneficial to human health. Lipids 2004, 39, 1197–1206. [Google Scholar] [CrossRef] [Green Version]
  42. Chilliard, Y.; Glasser, F.; Ferlay, A.; Bernard, L.; Rouel, J.; Doreau, M. Diet, rumen biohydrogenation and nutritional quality of cow and goat milk fat. Eur. J. Lipid Sci. Technol. 2007, 109, 828–855. [Google Scholar] [CrossRef]
  43. Chilliard, Y.; Glasser, F.; Enjalbert, F.; Ferlay, A.; Schmidely, P. Recent data on the effects of feeding factors on cow milk fatty acid composition. Sci. Aliment. 2008, 28, 156–167. [Google Scholar] [CrossRef] [Green Version]
  44. Kalač, P.; Samková, E. The effects of feeding various forages on fatty acid composition of bovine milk fat: A review. Czech J. Anim. Sci. 2010, 55, 521–537. [Google Scholar] [CrossRef] [Green Version]
  45. Flachowsky, G.; Erdmann, K.; Hüther, L.; Jahreis, G.; Möckel, P.; Lebzien, P. Influence of roughage/concentrate ratio and linseed oil on the concentration of trans-fatty acids and conjugated linoleic acid in duodenal chyme and milk fat of late lactating cows. Arch. Anim. Nutr. 2006, 60, 501–511. [Google Scholar] [CrossRef]
  46. Berthelot, V.; Albarello, H.; Broudiscou, L.P. Effect of extruded linseed supplementation, grain source and pH on dietary and microbial fatty acid outflows in continuous cultures of rumen microorganisms. Anim. Feed Sci. Technol. 2019, 249, 76–87. [Google Scholar] [CrossRef]
  47. Isenberg, B.J.; Soder, K.J.; Pereira, A.B.D.; Standish, R.; Brito, A.F. Production, milk fatty acid profile, and nutrient utilization in grazing dairy cows supplemented with ground flaxseed. J. Dairy Sci. 2019, 102, 1294–1311. [Google Scholar] [CrossRef] [Green Version]
  48. Resende, T.L.; Kraft, J.; Soder, K.J.; Pereira, A.B.D.; Woitschach, D.E.; Reis, R.B.; Brito, A.F. Incremental amounts of ground flaxseed decrease milk yield but increase n-3 fatty acids and conjugated linoleic acids in dairy cows fed high-forage diets1. J. Dairy Sci. 2015, 98, 4785–4799. [Google Scholar] [CrossRef] [PubMed]
  49. Lock, A.L.; Preseault, C.L.; Rico, J.E.; DeLand, K.E.; Allen, M.S. Feeding a C16: 0-enriched fat supplement increased the yield of milk fat and improved conversion of feed to milk. J. Dairy Sci. 2013, 96, 6650–6659. [Google Scholar] [CrossRef]
  50. Baumann, E.; Chouinard, P.Y.; Lebeuf, Y.; Rico, D.E.; Gervais, R. Effect of lipid supplementation on milk odd-and branched-chain fatty acids in dairy cows. J. Dairy Sci. 2016, 99, 6311–6323. [Google Scholar] [CrossRef]
  51. Jenkins, T.C.; Jenny, B.F. Nutrient digestion and lactation performance of dairy cows fed combinations of prilled fat and canola oil. J. Dairy Sci. 1992, 75, 796–803. [Google Scholar] [CrossRef]
  52. Emmanuel, B. The relative contribution of propionate, and long-chain even-numbered fatty acids to the production of long-chain odd-numbered fatty acids in rumen bacteria. Biochim. Biophys. Acta 1978, 528, 239–246. [Google Scholar] [CrossRef]
  53. Bauman, D.E.; Griinari, J.M. Regulation and nutritional manipulation of milk fat: Low-fat milk syndrome. Livest. Prod. Sci. 2001, 70, 15–29. [Google Scholar] [CrossRef]
  54. French, E.A.; Bertics, S.J.; Armentano, L.E. Rumen and milk odd-and branched-chain fatty acid proportions are minimally influenced by ruminal volatile fatty acid infusions. J. Dairy Sci. 2012, 95, 2015–2026. [Google Scholar] [CrossRef] [Green Version]
  55. Cívico, A.; Sánchez, N.N.; Gómez-Cortés, P.; Angel, M.; Fuente, D.; Blanco, F.P.; Angel, M. Odd-and branched-chain fatty acids in goat milk as indicators of the diet composition. Ital. J. Anim. Sci. 2017, 16, 68–74. [Google Scholar] [CrossRef]
  56. Prado, L.A.; Schmidely, P.; Nozière, P.; Ferlay, A. Milk saturated fatty acids, odd-and branched-chain fatty acids, and isomers of C18: 1, C18: 2, and C18: 3n-3 according to their duodenal flows in dairy cows: A meta-analysis approach. J. Dairy Sci. 2019, 102, 3053–3070. [Google Scholar] [CrossRef] [Green Version]
  57. Saliba, L.; Gervais, R.; Lebeuf, Y.; Chouinard, P.Y. Effect of feeding linseed oil in diets differing in forage to concentrate ratio: 1. Production performance and milk fat content of biohydrogenation intermediates of [alpha]-linolenic acid. J. Dairy Res. 2014, 81, 1–82. [Google Scholar] [CrossRef]
  58. Bayat, A.R.; Tapio, I.; Vilkki, J.; Shingfield, K.J.; Leskinen, H. Plant oil supplements reduce methane emissions and improve milk fatty acid composition in dairy cows fed grass silage-based diets without affecting milk yield. J. Dairy Sci. 2018, 101, 1136–1151. [Google Scholar] [CrossRef] [Green Version]
  59. Abu Ghazaleh, A.A. Effect of fish oil and sunflower oil supplementation on milk conjugated linoleic acid content for grazing dairy cows. Anim. Feed. Sci. Technol. 2008, 141, 220–232. [Google Scholar] [CrossRef]
  60. Harvatine, K.J.; Boisclair, Y.R.; Bauman, D.E. Recent advances in the regulation of milk fat synthesis. Animals 2009, 3, 40–54. [Google Scholar] [CrossRef] [Green Version]
  61. Kholif, A.E.; Morsy, T.A.; Abdo, M.M. Crushed flaxseed versus flaxseed oil in the diets of Nubian goats: Effect on feed intake, digestion, ruminal fermentation, blood chemistry, milk production, milk composition and milk fatty acid profile. Anim. Feed Sci. Technol. 2018, 244, 66–75. [Google Scholar] [CrossRef]
  62. Mach, N.; Zom, R.L.G.; Widjaja, H.C.A.; Van Wikselaar, P.G.; Weurding, R.E.; Goselink, R.M.A.; Van Vuuren, A.M. Dietary effects of linseed on fatty acid composition of milk and on liver, adipose and mammary gland metabolism of periparturient dairy cows. J. Anim. Physiol. Anim. Nutr. 2013, 97, 89–104. [Google Scholar] [CrossRef] [PubMed]
  63. Shingfield, K.J.; Bonnet, M.M.; Scollan, N.D. Recent developments in altering the fatty acid composition of ruminant-derived foods. Animal 2013, 7, 132–162. [Google Scholar] [CrossRef] [PubMed]
  64. Loor, J.J.; Ferlay, A.; Ollier, A.; Doreau, M.; Chilliard, Y. Relationship among trans and conjugated fatty acids and bovine milk fat yield due to dietary concentrate and linseed oil. J. Dairy Sci. 2005, 88, 726–740. [Google Scholar] [CrossRef] [Green Version]
  65. Loor, J.J.; Doreau, M.; Chardigny, J.M.; Ollier, A.; Sebedio, J.L.; Chilliard, Y. 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. Anim. Feed Sci. Technol. 2005, 119, 227–246. [Google Scholar] [CrossRef]
  66. Singh, A.P.; Avramis, C.A.; Kramer, J.K.G.; Marangoni, A.G. Algal meal supplementation of the cows’ diet alters the physical properties of milk fat. J. Dairy Res. 2004, 71, 66–73. [Google Scholar] [CrossRef] [PubMed]
  67. Maia, M.R.G.; Chaudhary, L.C.; Figueres, L.; Wallace, R.J. Metabolism of polyunsaturated fatty acids and their toxicity to the microflora of the rumen. Antonie Van Leeuwenhoek. 2007, 91, 303–314. [Google Scholar] [CrossRef] [PubMed]
  68. Halmemies-Beauchet-Filleau, A.; Kokkonen, T.; Lampi, A.-M.; Toivonen, V.; Shingfield, K.J.; Vanhatalo, A. Effect of plant oils and camelina expeller on milk fatty acid composition in lactating cows fed diets based on red clover silage. J. Dairy Sci. 2011, 94, 4413–4430. [Google Scholar] [CrossRef] [PubMed]
  69. Alfonso-Avila, A.R.; Baumann, E.; Charbonneau, É.; Chouinard, P.Y.; Tremblay, G.F.; Gervais, R. Interaction of potassium carbonate and soybean oil supplementation on performance of early-lactation dairy cows fed a high-concentrate diet. J. Dairy Sci. 2017, 100, 9007–9019. [Google Scholar] [CrossRef]
  70. Patel, M.; Wredle, E.; Bertilsson, J. Effect of dietary proportion of grass silage on milk fat with emphasis on odd-and branched-chain fatty acids in dairy cows. J. Dairy Sci. 2013, 96, 390–397. [Google Scholar] [CrossRef] [Green Version]
  71. Nielsen, T.S.; Sejrsen, K.; Andersen, H.R.; Lund, P.; Straarup, E.M. Effect of silage type and energy concentration on conjugated linoleic acid (CLA) in milk fat from dairy cows. J. Anim. Feed Sci. 2004, 13, 697–700. [Google Scholar] [CrossRef]
  72. Shingfield, K.J.; Reynolds, C.K.; Lupoli, B.; Toivonen, V.; Yurawecz, M.P.; Delmonte, P.; Beever, D.E. Effect of forage type and proportion of concentrate in the diet on milk fatty acid composition in cows given sunflower oil and fish oil. Anim. Sci. 2005, 80, 225–238. [Google Scholar] [CrossRef]
  73. Morales-Almaráz, E.; la Roza-Delgado, B.; González, A.; Soldado, A.; Rodriguez, M.L.; Peláez, M.; Vicente, F. Effect of feeding system on unsaturated fatty acid level in milk of dairy cows. Renew. Agric. Food Syst. 2011, 26, 224–229. [Google Scholar] [CrossRef]
  74. Bougouin, A.; Martin, C.; Doreau, M.; Ferlay, A. Effects of starch-rich or lipid-supplemented diets that induce milk fat depression on rumen biohydrogenation of fatty acids and methanogenesis in lactating dairy cows. Animal 2019, 13, 1421–1431. [Google Scholar] [CrossRef]
  75. Westreicher-Kristen, E.; Castro-Montoya, J.; Hasler, M.; Susenbeth, A. Relationship of milk odd-and branched-chain fatty acids with urine parameters and ruminal microbial protein synthesis in dairy cows fed different proportions of maize silage and red clover silage. Animals 2020, 10, 316. [Google Scholar] [CrossRef] [Green Version]
  76. Pi, Y.; Ma, L.; Pierce, K.M.; Wang, H.R.; Xu, J.C.; Bu, D.P. Rubber seed oil and flaxseed oil supplementation alter digestion, ruminal fermentation and rumen fatty acid profile of dairy cows. Animal 2019, 13, 2811–2820. [Google Scholar] [CrossRef] [PubMed]
  77. Zhang, Y.; Liu, K.; Hao, X.; Xin, H. The relationships between odd-and branched-chain fatty acids to ruminal fermentation parameters and bacterial populations with different dietary ratios of forage and concentrate. J. Anim. Physiol. Anim. Nutr. 2016, 101, 1103–1114. [Google Scholar] [CrossRef] [PubMed]
  78. Urrutia, N.; Bomberger, R.; Matamoros, C.; Harvatine, K.J. Effect of dietary supplementation of sodium acetate and calcium butyrate on milk fat synthesis in lactating dairy cows. J. Dairy Sci. 2019, 102, 5172–5181. [Google Scholar] [CrossRef]
  79. Kliem, K.E.; Humphries, D.J.; Kirton, P.; Givens, D.I.; Reynolds, C.K. Differential effects of oilseed supplements on methane production and milk fatty acid concentrations in dairy cows. Animal 2019, 13, 309–317. [Google Scholar] [CrossRef]
  80. Gómez-Cortés, P.; Civico, A.; de la Fuente, M.A.; Sánchez, N.N.; Blanco, F.P.; Marin, A.L.M. Effects of dietary concentrate composition and linseed oil supplementation on the milk fatty acid profile of goats. Animal 2018, 12, 2310–2317. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  81. De Carvalho, I.; da Fonseca, C.E.M.; Lopes, F.C.F.; Morenz, M.J.F.; da Gama, M.A.S.; de Souza, V.C.; da Silva, A.B. Milk fatty acid composition of dairy goats fed increasing levels of Flemingia macrophylla hay. Semin. Cienc. Agrar. 2019, 40, 293–310. [Google Scholar]
  82. Bainbridge, M.L.; Egolf, E.; Barlow, J.W.; Alvez, J.P.; Roman, J.; Kraft, J. Milk from cows grazing on cool-season pastures provides an enhanced profile of bioactive fatty acids compared to those grazed on a monoculture of pearl millet. Food Chem. 2017, 217, 750–755. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  83. Samková, E.; Špička, J.; Pešek, M.; Pelikánová, T.; Hanuš, O. Animal factors affecting fatty acid composition of cow milk fat: A review. S. Afr. J. Anim. Sci. 2012, 42, 83–100. [Google Scholar]
  84. Alberti, K.G.M.M.; Eckel, R.H.; Grundy, S.M.; Zimmet, P.Z.; Cleeman, J.I.; Donato, K.A.; Fruchart, J.-C.; James, W.P.T.; Loria, C.M.; Smith, S.C., Jr. Harmonizing the metabolic syndrome: A joint interim statement of the international diabetes federation task force on epidemiology and prevention; national heart, lung, and blood institute; American heart association; world heart federation; international atherosclerosis society; and international association for the study of obesity. Circulation 2009, 120, 1640–1645. [Google Scholar] [PubMed] [Green Version]
  85. Esposito, K.; Chiodini, P.; Colao, A.; Lenzi, A.; Giugliano, D. Metabolic syndrome and risk of cancer: A systematic review and meta-analysis. Diabetes Care 2012, 35, 2402–2411. [Google Scholar] [CrossRef] [Green Version]
  86. Miettinen, T.A.; Railo, M.; Lepäntalo, M.; Gylling, H. Plant sterols in serum and in atherosclerotic plaques of patients undergoing carotid endarterectomy. J. Am. Coll. Cardiol. 2005, 45, 1794–1801. [Google Scholar] [CrossRef]
  87. Manninen, V.; Tenkanen, L.; Koskinen, P.; Huttunen, J.K.; Mänttäri, M.; Heinonen, O.P.; Frick, M.H. Joint effects of serum triglyceride and LDL cholesterol and HDL cholesterol concentrations on coronary heart disease risk in the Helsinki Heart Study. Implications for treatment. Circulation 1992, 85, 37–45. [Google Scholar] [CrossRef] [Green Version]
  88. Reitz, C.; Tang, M.-X.; Luchsinger, J.; Mayeux, R. Relation of plasma lipids to Alzheimer disease and vascular dementia. Arch. Neurol. 2004, 61, 705–714. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  89. Cho, E.; Spiegelman, D.; Hunter, D.J.; Chen, W.Y.; Stampfer, M.J.; Colditz, G.A.; Willett, W.C. Premenopausal fat intake and risk of breast cancer. J. Natl. Cancer Inst. 2003, 95, 1079–1085. [Google Scholar] [CrossRef] [Green Version]
  90. Kroenke, C.H.; Kwan, M.L.; Sweeney, C.; Castillo, A.; Caan, B.J. High-and low-fat dairy intake, recurrence, and mortality after breast cancer diagnosis. J. Natl. Cancer Inst. 2013, 105, 616–623. [Google Scholar] [CrossRef] [Green Version]
  91. Kurotani, K.; Sato, M.; Yasuda, K.; Kashima, K.; Tanaka, S.; Hayashi, T. Even-and odd-chain saturated fatty acids in serum phospholipids are differentially associated with adipokines. PLoS ONE 2017, 12, e0178192. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  92. Rocha, D.M.; Caldas, A.P.; Oliveira, L.L.; Bressan, J.; Hermsdorff, H.H. Saturated fatty acids trigger TLR4-mediated inflammatory response. Atherosclerosis 2016, 244, 211–215. [Google Scholar] [CrossRef]
  93. Zong, G.; Li, Y.; Wanders, A.J.; Alssema, M.; Zock, P.L.; Willett, W.C.; Sun, Q. Intake of individual saturated fatty acids and risk of coronary heart disease in US men and women: Two prospective longitudinal cohort studies. Br. Med. J. 2016, 355, i5796. [Google Scholar] [CrossRef] [Green Version]
  94. Kim, Y.; Je, Y. Dairy consumption and risk of metabolic syndrome: A meta-analysis. Diabetic Med. 2016, 33, 428–440. [Google Scholar] [CrossRef] [PubMed]
  95. Bhupathi, V.; Mazariegos, M.; Rodriguez, J.B.C.; Deoker, A. Dairy intake and risk of cardiovascular disease. Curr. Cardiol. Rep. 2020, 22, 11. [Google Scholar] [CrossRef] [PubMed]
  96. Mitri, J.; Yusof, B.-N.M.; Maryniuk, M.; Schrager, C.; Hamdy, O.; Salsberg, V. Dairy intake and type 2 diabetes risk factors: A narrative review. Diabetes Metab. Syndr. Clin. Res. Rev. 2019, 13, 2879–2887. [Google Scholar] [CrossRef] [PubMed]
  97. White, M.J.; Armstrong, S.C.; Kay, M.C.; Perrin, E.M.; Skinner, A. Associations between milk fat content and obesity, 1999 to 2016. Pediatric Obes. 2020, 15, e12612. [Google Scholar] [CrossRef] [PubMed]
  98. Sun, Q.; Ma, J.; Campos, H.; Hu, F.B. Plasma and erythrocyte biomarkers of dairy fat intake and risk of ischemic heart disease. Am. J. Clin. Nutr. 2007, 86, 929–937. [Google Scholar] [CrossRef] [Green Version]
  99. Yu, E.; Hu, F.B. Dairy products, dairy fatty acids, and the prevention of cardiometabolic disease: A review of recent evidence. Curr. Atheroscler. Rep. 2018, 20, 1–9. [Google Scholar] [CrossRef]
  100. Yakoob, M.Y.; Shi, P.; Willett, W.C.; Rexrode, K.M.; Campos, H.; Orav, E.J.; Mozaffarian, D. Circulating biomarkers of dairy fat and risk of incident diabetes mellitus among men and women in the United States in two large prospective cohorts. Circulation 2016, 133, 1645–1654. [Google Scholar] [CrossRef] [Green Version]
  101. Santaren, I.D.; Watkins, S.M.; Liese, A.D.; Wagenknecht, L.E.; Rewers, M.J.; Haffner, S.M.; Hanley, A.J. Serum pentadecanoic acid (15:0), a short-term marker of dairy food intake, is inversely associated with incident type 2 diabetes and its underlying disorders. Am. J. Clin. Nutr. 2014, 100, 1532–1540. [Google Scholar] [CrossRef] [Green Version]
  102. Mozaffarian, D.; Cao, H.; King, I.B.; Lemaitre, R.N.; Song, X.; Siscovick, D.S.; Hotamisligil, G.S. Trans-palmitoleic acid, metabolic risk factors, and new-onset diabetes in US adults: A cohort study. Ann. Intern. Med. 2010, 153, 790–799. [Google Scholar] [CrossRef] [Green Version]
  103. De Oliveira Otto, M.C.; Nettleton, J.A.; Lemaitre, R.N.; Steffen, M.L.; Kromhout, D.; Rich, S.S.; Tsai, M.Y.; Jacobs, D.R.; Mozaffarian, D. Biomarkers of dairy fatty acids and risk of cardiovascular disease in the multi-ethnic study of atherosclerosis. J. Am. Heart Assoc. 2013, 2, e000092. [Google Scholar] [CrossRef] [Green Version]
  104. Venn-Watson, S.; Lumpkin, R.; Dennis, E.A. Efficacy of dietary odd-chain saturated fatty acid pentadecanoic acid parallels broad associated health benefits in humans: Could it be essential? Sci. Rep. 2020, 10, 1–14. [Google Scholar] [CrossRef]
  105. Aglago, E.K.; Biessy, C.; Torres-Mejia, G.; Angeles-Llerenas, A.; Gunter, M.J.; Romieu, I.; Chajès, V. Association between serum phospholipid fatty acid levels and adiposity in Mexican women. J. Lipid Res. 2017, 58, 1462–1470. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  106. Huang, L.; Lin, J.S.; Aris, I.M.; Yang, G.; Chen, W.Q.; Li, L.J. Circulating saturated fatty acids and incident type 2 diabetes: A systematic review and meta-analysis. Nutrients 2019, 11, 5. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  107. Jiménez-Cepeda, A.; Dávila-Said, G.; Orea-Tejeda, A.; González-Islas, D.; Elizondo-Montes, M.; Pérez-Cortes, G. Dietary intake of fatty acids and its relationship with FEV1/FVC in patients with chronic obstructive pulmonary disease. Clin. Nutr. ESPEN 2019, 29, 92–96. [Google Scholar] [CrossRef]
  108. Liu, S.; van der Schouw, Y.T.; Soedamah-Muthu, S.S.; Spijkerman, A.M.W.; Sluijs, I. Intake of dietary saturated fatty acids and risk of type 2 diabetes in the European Prospective Investigation into Cancer and Nutrition-Netherlands cohort: Associations by types, sources of fatty acids and substitution by macronutrients. Eur. J. Nutr. 2019, 58, 1125–1136. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  109. Matejcic, M.; Lesueur, F.; Biessy, C.; Renault, A.L.; Mebirouk, N.; Yammine, S. Circulating plasma phospholipid fatty acids and risk of pancreatic cancer in a large European cohort. Int. J. Cancer. 2018, 143, 2437–2448. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  110. Unger, A.L.; Torres-Gonzalez, M.; Kraft, J. Dairy fat consumption and the risk of metabolic syndrome: An examination of the saturated fatty acids in dairy. Nutrients 2019, 11, 2200. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  111. Villamor, E.; Villar, L.A.; Lozano-Parra, A.; Herrera, V.M.; Herrán, O.F. Serum fatty acids and progression from dengue fever to dengue haemorrhagic fever/dengue shock syndrome. Br. J. Nutr. 2018, 120, 787–796. [Google Scholar] [CrossRef] [Green Version]
  112. Yoo, W.; Gjuka, D.; Stevenson, H.L.; Song, X.; Shen, H.; Yoo, S.Y. Fatty acids in non-alcoholic steatohepatitis: Focus on pentadecanoic acid. PLoS ONE 2017, 12, e0189965. [Google Scholar] [CrossRef] [Green Version]
  113. Zhu, Y.; Tsai, M.Y.; Sun, Q.; Hinkle, S.N.; Rawal, S.; Mendola, P.; Zhang, C. A prospective and longitudinal study of plasma phospholipid saturated fatty acid profile in relation to cardiometabolic biomarkers and the risk of gestational diabetes. Am. J. Clin. Nutr. 2018, 107, 1017–1026. [Google Scholar] [CrossRef] [Green Version]
  114. Holman, R.T.; Johnson, S.B.; Kokmen, E. Deficiencies of polyunsaturated fatty acids and replacement by nonessential fatty acids in plasma lipids in multiple sclerosis. Proc. Natl. Acad. Sci. USA 1989, 86, 4720–4724. [Google Scholar] [CrossRef] [Green Version]
  115. Kurotani, K.; Karunapema, P.; Jayaratne, K.; Sato, M.; Hayashi, T.; Kajio, H. Circulating odd-chain saturated fatty acids were associated with arteriosclerosis among patients with diabetes, dyslipidemia, or hypertension in Sri Lanka but not Japan. Nutr. Res. 2018, 50, 82–93. [Google Scholar] [CrossRef] [PubMed]
  116. Fonteh, A.N.; Cipolla, M.; Chiang, J.; Arakaki, X.; Harrington, M.G. Human cerebrospinal fluid fatty acid levels differ between supernatant fluid and brain-derived nanoparticle fractions, and are altered in Alzheimer’s disease. PLoS ONE 2014, 9, e100519. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  117. Hodge, A.M.; English, D.R.; O’Dea, K.; Sinclair, A.J.; Makrides, M.; Gibson, R.A.; Giles, G.G. Plasma phospholipid and dietary fatty acids as predictors of type 2 diabetes: Interpreting the role of linoleic acid. Am. J. Clin. Nutr. 2007, 86, 189–197. [Google Scholar] [CrossRef] [Green Version]
  118. Meikle, P.J.; Wong, G.; Barlow, C.K.; Weir, J.M.; Greeve, M.A.; MacIntosh, G.L. Plasma lipid profiling shows similar associations with prediabetes and type 2 diabetes. PLoS ONE 2013, 8, e74341. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  119. Khaw, K.-T.; Friesen, M.D.; Riboli, E.; Luben, R.; Wareham, N. Plasma phospholipid fatty acid concentration and incident coronary heart disease in men and women: The EPIC-Norfolk prospective study. PLoS Med. 2012, 9, e1001255. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  120. Nestel, P.J.; Straznicky, N.; Mellett, N.A.; Wong, G.; De Souza, D.P.; Tull, D.L.; Meikle, P.J. Specific plasma lipid classes and phospholipid fatty acids indicative of dairy food consumption associate with insulin sensitivity. Am. J. Clin. Nutr. 2013, 99, 46–53. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  121. Mock, D.M.; Johnson, S.B.; Holman, R.T. Effects of biotin deficiency on serum fatty acid composition: Evidence for abnormalities in humans. J. Nutr. 1988, 118, 342–348. [Google Scholar] [CrossRef] [PubMed]
  122. Moser, H.W.; Moser, A.B.; Frayer, K.K.; Chen, W.; Schulman, J.D.; O’Neill, B.P.; Kishimoto, Y. Adrenoleukodystrophy: Increased plasma content of saturated very long chain fatty acids. Neurology 1981, 31, 1241. [Google Scholar] [CrossRef] [Green Version]
  123. Holman, R.T.; Adams, C.E.; Nelson, R.A.; Grater, S.J.E.; Jaskiewicz, J.A.; Johnson, S.B.; Erdman, J.W., Jr. Patients with anorexia nervosa demonstrate deficiencies of selected essential fatty acids, compensatory changes in nonessential fatty acids and decreased fluidity of plasma lipids. J. Nutr. 1995, 125, 901–907. [Google Scholar] [PubMed]
  124. Coker, M.; De Klerk, J.B.C.; Poll-The, B.T.; Huijmans, J.G.M.; Duran, M. Plasma total odd-chain fatty acids in the monitoring of disorders of propionate, methylmalonate and biotin metabolism. J. Inherit. Metab. Dis. 1996, 19, 743–751. [Google Scholar] [CrossRef] [PubMed]
  125. Stefanov, I.; Baeten, V.; Abbas, O.; Colman, E.; Vlaeminck, B.; De Baets, B.; Fievez, V. Analysis of milk odd-and branched-chain fatty acids using Fourier transform (FT)-Raman spectroscopy. J. Agric. Food Chem. 2010, 58, 10804–10811. [Google Scholar] [CrossRef]
  126. Yang, Z.; Liu, S.; Chen, X.; Chen, H.; Huang, M.; Zheng, J. Induction of apoptotic cell death and in vivo growth inhibition of human cancer cells by a saturated branched-chain fatty acid, 13-methyltetradecanoic acid. Cancer Res. 2000, 60, 505–509. [Google Scholar]
  127. Cai, Q.; Huang, H.; Qian, D.; Chen, K.; Luo, J.; Tian, Y.; Lin, T.; Lin, T. 13-Methyltetradecanoic acid exhibits anti-tumor activity on T-cell lymphomas in vitro and in vivo by down-regulating p-AKT and activating caspase-3. PLoS ONE 2013, 8, e65308. [Google Scholar] [CrossRef] [PubMed]
  128. Ran-Ressler, R.R.; Khailova, L.; Arganbright, K.M.; Adkins-Rieck, C.K.; Jouni, Z.E.; Koren, O.; Dvorak, B. Branched chain fatty acids reduce the incidence of necrotizing enterocolitis and alter gastrointestinal microbial ecology in a neonatal rat model. PLoS ONE 2011, 6, e29032. [Google Scholar] [CrossRef] [Green Version]
  129. Wongtangtintharn, S.; Oku, H.; Iwasaki, H.; Toda, T. Effect of branched-chain fatty acids on fatty acid biosynthesis of human breast cancer cells. J. Nutr. Sci. Vitaminol. 2004, 50, 137–143. [Google Scholar] [CrossRef] [Green Version]
  130. Kraft, J.; Jetton, T.; Satish, B.; Gupta, D. Dairy-derived bioactive fatty acids improve pancreatic ß-cell function. FASEB J. 2015, 29, 608–625. [Google Scholar] [CrossRef]
  131. Kuhajda, F.P. Fatty-acid synthase and human cancer: New perspectives on its role in tumor biology. Nutrition 2000, 16, 202–208. [Google Scholar] [CrossRef]
  132. Astrup, A.; Geiker, N.R.W.; Magkos, F. Effects of full-fat and fermented dairy products on cardiometabolic disease: Food is more than the sum of its parts. Adv. Nutr. 2019, 10, 924S–930S. [Google Scholar] [CrossRef] [PubMed]
  133. Kratz, M.; Baars, T.; Guyenet, S. The relationship between high-fat dairy consumption and obesity, cardiovascular, and metabolic disease. Eur. J. Nutr. 2013, 52, 1–24. [Google Scholar] [CrossRef] [PubMed]
Animals 11 03210 g001 550
Figure 1. Origin of milk odd and branched chain fatty acids.
Figure 1. Origin of milk odd and branched chain fatty acids.
Animals 11 03210 g001
Table
Table 1. Summary of the effects of lipid supplements and forage proportions on OBCFAs synthesis in the rumen of dairy cows.
Table 1. Summary of the effects of lipid supplements and forage proportions on OBCFAs synthesis in the rumen of dairy cows.
ReferencesAmounts of Lipid Supplements or Forage RatioAnimal BreedObserved Effects on Rumen OBCFAs
[46]10% of DM of LW(extruded linseed and wheat) or LC (extruded linseed and corn)Holstein cowsLW: OCFAs↓, iso FA↑, anteiso FA↓.
LC: OBCFAs ↓.
[76]4% RSO (rubber seed oil), 4% FSO or RFO (rubber seed oil + flaxseed oil)Holstein cowsRSO: C15:0↓, C17:0↓.
FSO: C15:0↓, C17:0↓.
RFO: C15:0↓, C17:0↓.
[77]30:70, 50:50 and 70:30 forage: concentrate ratio (F:C)Holstein cows70:30: C11:0↑, C13:0↑, iso C15:0↑, iso C16:0↑, iso C17:0↑ and C17:0↑
70:30: anteiso C15:0↓, C15:0↓and total OBCFAs↓
[54]Infusion of 18.8 mol of AC (acetate), PR (propionate), IV (isovalerate) and AIV (anteisovalerate)Holstein cowsAIV: iso C15:0↑ and C17:0↑ in rumen liquid
AIV: anteiso C15:0↑ and anteiso C17:0↑ in rumen solid
IV: iso C15:0↑ in rumen solids
AC: acetate; AIV: anteisovalerate; Decrease: (↓); DM: Dry matter; FA: fatty acids; F:C: forage: concentrate ratio; FSO: flaxseed oil; Increase: (↑); IV: isovalerate; LC: extruded linseed and corn; LW: extruded linseed and wheat; LW: OCFAs↓ = LW decrease OCFAs; No effect: (↔); OCFAs: odd chain fatty acids; PR: propionate; RFO: rubber seed oil + flaxseed oil; RSO: rubber seed oil.
Table
Table 2. Summary of the effects of lipid supplements on milk OBCFAs in dairy cows.
Table 2. Summary of the effects of lipid supplements on milk OBCFAs in dairy cows.
ReferencesConcentrationsor Amounts of Lipid SupplementAnimal BreedsObserved Effects on Milk OBCFAs
[47]GFS (Ground flaxseed) 10% of TMR (total mixed ration)Jersey cows11:0↓, 13:0↓, 15:0↓, 17:0↓, iso 14:0↓, iso 15:0↓, anteiso15:0↓, iso 16:0↓, iso 17:0↑, anteiso 17:0↓ (ΣOBCFAs↓).
[78]2.9% sodium AC (acetate) and 2.5% calcium BU (butyrate) in a diet.Holstein cowsAcetate: ΣOBCFAs↓.
Butyrate: ΣOBCFAs (↔).
[79]22 g oil/kg diet DM (Dry matter) of EL (Extruded linseed), CPLO (calcium salts of palm and linseed) or MR (milled rapeseed)Holstein Friesian cowsEL: 13:0↓, iso13:0↔, anteiso13:0↓, iso14:0↓, 15:0↓, anteiso15:0↓, iso16:0↓, 17:0↓, iso17:0↑, iso18:0↑.
CPLO: 13:0↓, iso13:0↔, anteiso13:0↓, iso14:0↓, 15:0↓, anteiso15:0↓, iso16:0↓, 17:0↓, iso17:0↓, iso18:0↑.
MR: 13:0↓, iso13:0↔, anteiso13:0↓, iso14:0↔, 15:0↓, anteiso15:0↓, iso16:0↓, 17:0↓, iso17:0↓, iso18:0↑.
[16]30 g/kg of Prilled palm fat (PPF)/+ Sunflower oil (SO)Holstein cowsSO: anteiso13:0↓, anteiso15:0↓, 15:0↓, 17:0↓, cis-9 15:1↓, and cis917:1↓;
PPF+SO: iso14:0↑ and iso16:0↑
[80]30 g/day of LO: linseed oil (S/LO: high starch plus linseed oil and F/LO: high non-forage plus linseed oil treatments).Malagueña goatsS/LO: Total odd↑, Total iso↓, Total anteiso↑.
F/LO: Total odd↓, Total iso↓, Total anteiso↓.
[69]2% of Soybean oil (SBO)Holstein cowsiso 13:0↑, 11:0↓, anteiso 13:0↔, 13:0↓, iso 14:0↓, iso 15:0↓, anteiso 15:0↓, 15:0↓, iso 16:0↑, iso 17:0↑, anteiso 17:0↓, 17:0↓, cis-7 17:0↓, cis-8 17:1↓, cis-9 17:1↓, iso 18:0↓, 19:0↓.
[69]2% SBO (Soybean oil) +1.5% Potassium carbonate (K2CO3)Holstein cowsiso 13:0↑, 11:0↓, anteiso 13:0↓, 13:0↓, iso 14:0↓, iso 15:0↓, anteiso 15:0↓, 15:0↓, iso 16:0↓, iso 17:0↓, anteiso 17:0↑, 17:0↓, cis-7 17:0↓, cis-8 17:1↓, cis-9 17:1↓, iso 18:0↓, 19:0↑.
[50]450 g/d of CTL (lipid free emulsion medium injected into the rumen), RSO (lipid free emulsion medium injected into the rumen), RSF (saturated fatty acids injected into the rumen), ASF (saturated fatty acids injected into the abomasum)Holstein cowsRSO: OCFAs↓, ECisoFAs↔
RSF: 17:0+cis-9 17:1↑
RSF and ASF: OBCFAs ↔
[48]0, 5, 10 and 15% of GFS (Ground flaxseed)Jersey cowsGFS: OBCFAs↓ linearly
[54]An Infusion of 18.8 mol of AC (acetate), PR (propionate), IV (isovalerate) and AIV (anteisovalerate)Holstein cowsPR: C15:0↑ and C17:0↑;
IV: iso C15:0↑;
AIV: C15:0↑
[68]29g/kg of Plant oilsAyrshire cowsOBCFAs↓
AC: acetate (eg: Acetate: ΣOBCFAs↓ = Acetate decrease the sum of OBCFAs); AIV: anteisovalerate; ASF: saturated fatty acids injected into the abomasum; BU: butyrate; CTL: lipid free emulsion medium injected into the rumen; Decrease: (↓); DM: dry matter; ECFAs: even chain fatty acids; EL: Extruded linseed ; F/LO: high non-forage plus linseed oil; GFS: Ground flaxseed; Increase: (↑); IV: isovalerate; limited effect or no effect: (↔); LO: linseed oil; PPF: Prilled palm fat; PR: propionate; RSF: saturated fatty acids injected into the rumen; RSO: soybean oil injected into the rumen; S/LO: high starch plus linseed oil; SBO: Soybean oil) ; SO: Sunflower oil; TMR: Total mixed ration; Vegetable oils: sunflower seed oil, rapeseed oil, camelina seed oil or camelina expeller.
Table
Table 3. Summary of the effects of proportion, type of forage, and forage-to-concentrate ratio on milk OBCFAs in ruminants.
Table 3. Summary of the effects of proportion, type of forage, and forage-to-concentrate ratio on milk OBCFAs in ruminants.
ReferenceType or Amount of Forage in g/Kg or %Species or Breed of AnimalObserved Effects on Milk OBCFAs
[81]IA (incremental amount) of FMH (Flemingia macrophylla hay): 0, 80, 160, 240
and 320 g kg-1 DM (dry matter)		Saanen x Boer goats80: Σ OBCFAs↓
160: Σ OBCFAs↑,
240: Σ OBCFAs↓,
320: ΣOBCFAs↑
[16]F:C (forage: concentrate ratio) 39:61, 44:56, or 48:52Holstein cowsForage: OBCFAs↑
[82]A 0.5 ha paddock of CSP and two
0.25 ha paddocks 22.4 kg/ha with PM		Holstein cowsPM: OBCFAs↑
[70]With incremental amount of grass silage: 50, 70 and 85%The Swedish Red Breed of cowsC15:0↑, C17:0↑, iso C15:0↑
and total OBCFAs↑
CSP: cool season pasture; Decrease: (↓); DM: dry matter; F:C: forage: concentrate ratio; FMH: Flemingia macrophylla hay; IA: incremental amount; Increase: (↑); No effect: (↔); PM: warm-season monoculture of pearl millet.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Abdoul-Aziz, S.K.A.; Zhang, Y.; Wang, J. Milk Odd and Branched Chain Fatty Acids in Dairy Cows: A Review on Dietary Factors and Its Consequences on Human Health. Animals 2021, 11, 3210. https://doi.org/10.3390/ani11113210

AMA Style

Abdoul-Aziz SKA, Zhang Y, Wang J. Milk Odd and Branched Chain Fatty Acids in Dairy Cows: A Review on Dietary Factors and Its Consequences on Human Health. Animals. 2021; 11(11):3210. https://doi.org/10.3390/ani11113210

Chicago/Turabian Style

Abdoul-Aziz, Sidi Ka Amar, Yangdong Zhang, and Jiaqi Wang. 2021. "Milk Odd and Branched Chain Fatty Acids in Dairy Cows: A Review on Dietary Factors and Its Consequences on Human Health" Animals 11, no. 11: 3210. https://doi.org/10.3390/ani11113210

APA Style

Abdoul-Aziz, S. K. A., Zhang, Y., & Wang, J. (2021). Milk Odd and Branched Chain Fatty Acids in Dairy Cows: A Review on Dietary Factors and Its Consequences on Human Health. Animals, 11(11), 3210. https://doi.org/10.3390/ani11113210

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop