Lipids (2014) 49:275–286 DOI 10.1007/s11745-013-3876-1
ORIGINAL ARTICLE
Types of Oilseed and Adipose Tissue Influence the Composition and Relationships of Polyunsaturated Fatty Acid Biohydrogenation Products in Steers Fed a Grass Hay Diet C. Mapiye • J. L. Aalhus • T. D. Turner • D. C. Rolland • J. A. Basarab • V. S. Baron • T. A. McAllister • H. C. Block S. D. Proctor • M. E. R. Dugan
•
Received: 6 August 2013 / Accepted: 20 December 2013 / Published online: 8 January 2014 Ó Her Majesty the Queen in Right of Canada 2014
Abstract The current study evaluated the composition and relationships of polyunsaturated fatty acid biohydrogenation products (PUFA-BHP) from the perirenal (PRF) and subcutaneous fat (SCF) of yearling steers fed a 70 % grass hay diet with concentrates containing either sunflower-seed (SS) or flaxseed (FS). Analysis of variance indicated several groups or families of structurally related FA, and individual FA within these were affected by a number of novel oilseed by fat depot interactions (P \ 0.05). Feeding diets containing SS increased the proportions of non-conjugated 18:2 BHP (i.e., atypical dienes, AD) and conjugated linoleic acids (CLA) with the first double bond from carbon 7 to 9, trans-18:1 isomers
C. Mapiye J. L. Aalhus T. D. Turner D. C. Rolland V. S. Baron M. E. R. Dugan (&) Agriculture and Agri-Food Canada, Lacombe Research Centre, 6000 C and E Trail, Lacombe, AB T4L 1W1, Canada e-mail:
[email protected] J. A. Basarab Alberta Agriculture and Rural Development, Lacombe Research Centre, 6000 C and E Trail, Lacombe, AB T4L 1W1, Canada T. A. McAllister Agriculture and Agri-Food Canada, Lethbridge Research Centre, 1st Avenue South 5403, P.O. Box 3000, Lethbridge, AB T1J 4B1, Canada H. C. Block Agriculture and Agri-Food Canada, Brandon Research Centre, 18th Street and Grand Valley Road, P.O. Box 1000A, RR3, Brandon, MB R7A 5Y3, Canada S. D. Proctor Metabolic and Cardiovascular Diseases Laboratory, Alberta Diabetes and Mazankowski Institutes, Li Ka Shing Centre for Health Research Innovation, University of Alberta, Edmonton, AB T6G 2E1, Canada
with double bonds from carbon 6 to 12, and these PUFABHP had greater proportions in SCF compared to PRF (P \ 0.05). Enrichment of conjugated linolenic acids, AD and CLA isomers with the first double bond in position 11 or 12, and t-18:1 isomers with double bonds from carbon 13 to 16 were achieved by feeding diets containing FS, with PRF having greater proportions than SCF (P \ 0.05). Principal component analysis visually confirmed interaction effects on these groups/families of FA, and further confirmed or suggested a number of relationships between PUFA-BHP. Feeding SS or FS in a grass hay diet and exploiting adipose tissue differences, therefore, present unique opportunities to differentially enrich a number of PUFA-BHP which seem to have positive health potential in humans (i.e., t11-18:1, c9,t11-18:2 and c9,t11,c15-18:3). Keywords Adipose tissue Beef Grass hay Lipids Oilseed Rumenic acid Vaccenic acid Abbreviations ALA a-Linolenic acid ANOVA Analysis of variance AD Atypical dienes BCFA Branched-chin fatty acids BHP Biohydrogenation products c Cis CLA Conjugated linoleic acids CLNA Conjugated linolenic acids DM Dry matter FA Fatty acids FAME Fatty acid methyl esters GC Gas chromatography FS Flaxseed GH Grass hay LA Linoleic acid
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n-3 n-6 PRF PUFA PCA RC SCF SS SFA t
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Omega-3 Omega-6 Perirenal fat Polyunsaturated fatty acids Principal component analysis Red clover silage Subcutaneous fat Sunflower-seed Saturated fatty acids Trans
and relationships of PUFA-BHP differ between subcutaneous fat (SCF) and perirenal fat (PRF) of yearling steers fed a GH diet with either SS or FS as the PUFA source. Such information can be utilised to adopt a diet that increases the levels of specific PUFA-BHP in the adipose tissues and would enable sorting of trim fat according to adipose tissue type to optimise the functional potential of processed beef products. In addition, elevated levels of particular PUFA-BHP together with the information on relationships could be useful in the evaluation of safety and/or health effects of individual and/or groups of PUFA-BHP.
Introduction Materials and Methods Beef is a nutritious food and its consumption has recently been recognized as a way to combat muscle wasting in elderly people [1], but still suffers the stigma of containing upwards of 40 % saturated fatty acids (SFA) [2]. This includes *4 % myristic (14:0) and *25 % palmitic acids (16:0), both of which have been associated with cardiovascular diseases in humans relating to their low-density lipoprotein cholesterol-raising properties [3]. Nevertheless, beef fat also contains polyunsaturated fatty acid biohydrogenation products (PUFA-BHP), particularly rumenic acid (c9,t11-18:2) and its precursor vaccenic acid (t11-18:1), which exhibit potentially beneficial effects on human health [4, 5]. In this regard, several dietary strategies have been evaluated for their potential to increase the levels of these potentially beneficial PUFA-BHP in beef [6, 7]. To this end, supplementing high-forage diets with rich sources of linoleic acid (18:2n-6, LA) such as sunflower-seed (SS) was found to be effective at increasing t11-18:1 and c9,t11-18:2 in beef tissues [8], whereas sources rich in a-linolenic acid (18:3n-3, ALA) such as flaxseed (FS) also increase ALA specific BHP including conjugated linolenic acids (CLNA) and non-conjugated 18:2 BHP (i.e., atypical dienes, AD) [9, 10] whose human health effects have not been elucidated. Research indicates that apart from the forage level, the type of forage also influences the composition of PUFA-BHP in beef [11]. Our recent studies have demonstrated that grass hay (GH) is superior to barley silage for enhancing levels of PUFA-BHP in beef, including t11-18:1 and c9,t11-18:2 when feeding FS [9, 12]. In addition, there is evidence that the deposition of PUFABHP varies with adipose tissue type [10, 13]. The interactive effects of oilseed source and adipose tissue type on the accumulation of PUFA-BHP in beef cattle fed a high-forage diet, GH in particular, are limited if any. The current study examines how the proportions
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Animals and Nutrient Composition of the Experimental Diets Animal management, ingredient and nutritional composition of the experimental diets were previously described by Mapiye et al. [14]. Briefly, 32 crossbred steers were stratified by weight to two experimental diets (GH-FS, GH-SS), with two pens of eight steers per diet. On a dry matter (DM) basis, diets contained 70 % GH and concentrates containing either SS (18.4 %) or FS (14.3 %), each providing 5.4 % oil to the diets. In an attempt to equalise the digestible energy of the diets, additional ground barley grain (7.4 %) was added to the diets containing SS, and additional barley straw (11.2 %) was added to the diets containing FS. Flaxseed was triple rolled, while SS was fed whole. The content of crude protein (13.3 %), crude fat (6.5 %), acid detergent fibre (44.9 %), neutral detergent fibre (55.4 %), calcium (1.1 %), phosphorous (0.3 %) and digestible energy (2.1 Mcal/kg) were similar across dietary treatments. The major FA in the FS and SS containing diets were ALA (50 % of total FA) and LA (66 %), respectively. Sample Collection Steers were slaughtered at the Lacombe Research Centre abattoir over four slaughter dates in November 2011 (two steers/pen/diet/slaughter day) at an average of 205 days on feed corresponding to SCF depths of 5–8 mm between the 12th and 13th rib over the right longissimus thoracis muscle of each animal. At slaughter, steers were stunned, exsanguinated and dressed in a commercial manner. About 20 min postmortem, during evisceration, samples of PRF closest to the cranial-central part of the whole PRF and SCF adjacent to the 12th rib were collected for FA analysis.
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Fatty Acid Analysis
Results
PRF and SCF samples (50 mg) were freeze-dried and directly methylated with sodium methoxide [15]. Internal standard, 1 ml of 1 mg c10-17:1 methyl ester/ml toluene (standard no. U-42M form Nu-Check Prep Inc., Elysian, MN, USA) was added prior to addition of methylating reagents. Fatty acid methyl esters (FAME) were analysed by gas chromatography (GC) using a CP-Sil88 column (100 m, 25 lm ID, 0.2 lm film thickness) in a CP-3800 gas chromatograph equipped with an 8600-series autosampler (Varian Inc., Walnut Creek, CA, USA). Two GC FAME analyses were conducted per sample using complementary temperature programs with 150 and 175 °C plateaus according to Kramer et al. [17]. CLA isomers not separated by GC were further analysed using Ag?-HPLC as described by Cruz-Hernandez et al. [16]. Individual peaks for the majority of FAME were identified using the reference standard no. 601 from Nu-Check Prep Inc., Elysian, MN, USA. CLA isomers were identified using a UC-59M standard from Nu-Chek Prep Inc., which contains all four positional CLA isomers. Trans-18:1, CLA, AD, and CLNA isomers not included in the standard mixtures were identified by their retention times and elution order as reported in the literature [16–18]. The FAME were quantified using chromatographic peak area and internal standard based calculations. Fatty acid groups [n-6 PUFA, n-3 PUFA, CLNA, AD, CLA, c-18:1, t-18:1, branched chain FA (BCFA) and SFA] were expressed as mole percentage of total FA identified while individual PUFA-BHP were expressed as a percentage of their respective FA group.
Effects of Types of Oilseed and Adipose Tissue on Fatty Acid Groups
Statistical Analysis Fatty acids were analysed using the PROC MIXED procedure of SAS [19]. The model included oilseed, tissue and their interaction as fixed effects and random effects of slaughter date, pen and animal nested within the oilseed 9 tissue interaction. Since the random effect of pen was not significant, it was removed from the FA models and individual animal was used as the experimental unit. Treatment means were generated and separated using the LSMEANS and PDIFF options, respectively. Principal component analysis (PCA) was performed using the PRINCOMP procedure of SAS [19] to determine the pattern of inter-correlations among PUFA-BHP (variables) and variability of samples in relation to the types of oilseed fed and adipose tissue sampled. Loadings plots derived from PCA were used to identify correlations among PUFA-BHP whereas score plots were used to illustrate variability among samples. Interrelationships between samples and variables were identified by comparing PCA loading and score plots.
Total FA content was only influenced by adipose tissue type, with PRF having greater (P \ 0.05) content than SCF (Table 1). Regardless of the oilseed fed, of the FA groups, total SFA was the dominant group contributing about 38 and 54 % of total FA in SCF and PRF, respectively followed by c-18:1 contributing about 46 and 25 % of total FA in SCF and PRF, respectively (Table 1). Trans-18:1 contributed 6–8 and 8–15 % of the total FA in SCF and PRF, respectively (Table 1). The remaining groups (n-6 PUFA, n-3 PUFA, CLNA, AD, CLA and BCFA) contributed \3 % of the total FA each regardless of the adipose tissue type (Table 1). The proportions of total n-6 PUFA tended to be greater (P \ 0.07) in SCF than in PRF (Table 1). A differential response to oilseed type was detected in the adipose tissues for total n-3 PUFA, AD, total CLA and total t-18:1 (P \ 0.05; Table 1). The PRF from steers fed FS had the greatest proportions of total n-3 PUFA, followed by SCF from steers fed FS (P \ 0.05), whereas PRF and SCF from steers fed SS had the lowest proportions with no significant difference found between them (P [ 0.05). For AD, PRF from steers fed FS and SCF from steers fed FS had the greatest proportions followed by SCF from steers fed SS and PRF from steers fed SS (P \ 0.05). Subcutaneous fat from steers fed the SS containing diet had the largest proportions of total CLA followed by SCF from steers fed FS, and PRF from steers fed FS and SS diets had the lowest proportions (P \ 0.05). For total t-18:1, PRF from steers fed SS had the greatest proportions followed by PRF from steers fed FS, SCF from steers fed SS and SCF from steers fed FS (P \ 0.05; Table 1). Only, oilseed type affected the proportions of total CLNA, with steers fed FS having greater (P \ 0.05) proportions than steers fed SS (Table 1). The proportions of total BCFA tended to be greater (P \ 0.06) in FS steers than in SS steers (Table 1). Subcutaneous fat had greater (P \ 0.05) proportions of total c-18:1 and lower (P \ 0.05) proportions of total SFA compared to PRF (Table 1).
Effects of Types of Oilseed and Adipose Tissue on Individual PUFA-BHP CLNA isomers were dominated by c9,t11,c15-18:3, making up 60–80 % of total CLNA irrespective of the adipose tissue type and oilseed fed (Table 1). Oilseed effects were significant for the individual CLNA isomers (P \ 0.05;
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Table 1 Effects of types of oilseed and adipose tissue on fatty acid profiles of yearling steers fed a grass hay diet Variable
Total fatty acids (mg/g fat)
Subcutaneous fat
Perirenal fat
Flaxseed
Sunflower-seed
Flaxseed
Sunflower-seed
908
890
956
946
Fatty acid groups (mol% of total fatty acids) P n-6 1.50 P n-3 0.60b P CLNA 0.30 P AD 2.70a P CLA 2.20b P cis-18:1 46.6 P trans-18:1 6.40d P BCFA 2.10 P SFA 37.7
1.80
1.30
c
a
SEM
1.70 c
P values O
T
O9T
0.02
0.39
0.003
0.82
0.10
0.16
0.07
0.61
0.40
0.70
0.40
0.10
0.02
0.03
0.04
0.10
0.30
0.10
0.10
0.04
0.97
0.82
1.70b
2.70a
1.00c
0.20
0.03
0.001
0.001
a
c
1.70 26.7
1.40c 24.8
0.20 0.90
0.52 0.16
0.001 0.001
0.004 0.45
8.40c
10.8b
14.7a
0.50
0.02
0.001
0.01
2.10
1.80
0.10
0.06
0.56
0.20
2.60 46.0
1.90 37.0
53.6
53.9
1.00
0.79
0.001
0.57
0.03
0.001
0.45
Conjugated linolenic acid isomers (% of total CLNA) c9,t11,c15
63.9
60.3
80.8
78.5
0.96
c9,t11,t15
36.1
39.7
19.2
21.5
0.82
0.04 0.001 0.69 P Means with differentP superscripts letters for a particular fatty acidPprofile are significantly different (P \ 0.05); P n-6 = sum of 18:2n-6, 20:2n6, 20:3n-6, 20:4n-6; n-3 = sum of 18:3n-3, 20:3n-3, 22:5n-3; CLNA = sum of c9,t11,t15-, P c9,t11,c15-; AD total atypical dienes = sum of t11,t15-, c9,t13-/t8,c12-, t8,c13-, P c9,t12-/c16-18:1, t9,c12-, t11,c15-, c9,c15-, c12,c15-; CLA = sum P of t7,c9-, t8,c10-, c9,t11-, t9,c11-, t10,c12-, t10,t12-, t11,t13-, t12,t14; t-18:1 = sum of t6-/t7-/t8-, t9-, t10-, t11-, t12-, t13-/t14-, t15-, t16-; c-MUFA = sum P of c9-14:1, c716:1, c9-16:1, c11-16:1, c9-17:1, c9-18:1, c11-18:1, c12-18:1, c13-18:1, c14-18:1, c15-18:1, c16-18:1, c9-20:1, c11-20:1; BCFA = sum of P iso-15:0, anteiso15:0, iso16, iso17:0, anteiso17:0, iso18:0; SFA = sum of 14:0, 15:0, 16:0, 17:0, 18:0, 19:0, 20:0, 22:0 SEM standard error of mean, O oilseed effect, T tissue effect, O 9 T Oilseed by tissue interaction
Table 1). The proportions of c9,t11,c15-18:3 in total CLNA were greater (P \ 0.05) when the diet contained FS, while the proportions of c9,t11,t15-18:3 in total CLNA were greater (P \ 0.05) when the diet contained SS (Table 1). Perirenal fat had greater (P \ 0.05) and smaller (P \ 0.05) proportions of c9,t11,c15-18:3 and c9,t11,t1518:3, respectively. However, adipose tissue effects were of greater magnitude than oilseed effects. Proportionally, t11,c15-18:2 was the major AD isomer in SCF from FS fed steers and PRF from FS and SS fed steers and constituted about 30–50 % of total AD whereas t8,c12-18:2 was the dominant isomer in SCF from SS fed steers and constituted about 30 % of total AD (Fig. 1a). A significant oilseed 9 tissue interaction was observed for t11,t15-18:2 indicating its proportions were greatest in PRF from FS fed steers followed by PRF from SS fed steers, SCF from FS fed steers and SCF from SS fed steers (P \ 0.05; Fig. 1a). Individual AD isomers with the first double bond at carbon 11 or 12 (t11,c15-; t11,t15-; c12,c15-18:2) were influenced by both oilseed and adipose tissue type, with steers fed FS vs. SS, and PRF vs. SCF having greater proportions of these isomers (P \ 0.05; Fig. 1a). Oilseed 9 tissue interactions (P \ 0.05) were detected for t9,c12- and t9,t12-/c9,t13-18:2. The proportions of t9,c12-18:2 were greatest in PRF from steers fed SS followed by SCF from steers fed SS, PRF from steers fed FS
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and SCF from steers fed FS (P \ 0.05; Fig. 1a). Subcutaneous fat from steers fed SS had the greatest proportions of t9,t12-/c9,t13-18:2 followed by PRF from steers fed SS, SCF from steers fed FS and PRF from steers fed FS (P \ 0.05; Fig. 1a). Oilseed and tissue effects were significant (P \ 0.05) for t8,c12-; t8,c13-; c9,t12-; c9,c1518:2 (Fig. 1a) with feeding SS vs. FS, and SCF vs. PRF having greater (P \ 0.05) proportions. The most concentrated CLA isomer found when feeding SS was c9,t11-18:2, and it reached a high of 82 % of total CLA in SCF (Fig. 1b). Oilseed 9 tissue interactions (P \ 0.05) occurred for all the identified CLA isomers (Fig. 1b). Overall, PRF from steers fed FS had the greatest proportions of CLA isomers (% total CLA) with the first double bond at carbon 11 or 12 (c11,t13-; t11,c13-; t11,t13-; t12,t14-; t12,c14-; c12,t14-18:2), SCF from steers fed SS had the lowest proportions while SCF from steers fed FS and PRF from steers fed SS had intermediate proportions (P \ 0.05; Fig. 1b). On the other hand, steers fed SS had greater (P \ 0.05) proportions of individual CLA isomers (% total CLA) with the first double bond located from carbon 7 to 10, but PRF had greater (P \ 0.05) proportions of t8,c10-; t9,t11-; t10,c12- and t10,t12-18:2 while SCF had greater (P \ 0.05) proportions of t7,c9-; t9,c11and c9,t11-18:2 (Fig. 1b). Oleic acid (c9-18:1) was the principal c-18:1 isomer contributing 75–80 % of total c-18:1 isomers regardless of
Lipids (2014) 49:275–286
% of total atypical dienes
A
279
55 50 45 40 35 30 25 20 15 10 5 0
a a
d
d c b
t8,c12
t8,c13
c9,t12
a
b
c
b
bc c
t9,c12
t9,t12/c9,t13
c9,c15
t11,c15
t11,t15
c12,c15
% of total conjugated linoleic acids
B 85 80 75 70 65 60 55 50 45 15 10 5 0
a b
b
c a a
dc
ccba
t7,c9
t8,c10
b
a a
b
c9,t11
Subcutaneous fat-Flaxseed
ab a c b
cdca
t9,c11
t9,t11
cbb
a
c bb
a
bcac
c
b bc
c
b
bcab
b c a b bc c
b
t10,c12 t10,t12 c11,t13 t11,c13 t11,t13 c12,t14 t12,c14 t12,t14
Subcutaneous fat-Sunflower-seed
Perirenal fat-Flaxseed
Perirenal fat-Sunflower-seed
Fig. 1 Effects of types of oilseed and adipose tissue on atypical dienes (a) and conjugated linoleic acids (b) isomers from yearling steers fed a grass hay diet. Means with different letters (a–d) for a
particular biohydrogenation product are significantly different (P \ 0.05); a significant oilseed effect (P \ 0.05); b significant tissue effect (P \ 0.05)
the adipose tissue type and oilseed fed (Fig. 2a). Oilseed 9 tissue interactions were significant for several c-18:1 isomers (c9-; c11-; c12-18:1; Fig. 2a). Subcutaneous fat from steers fed FS had the largest proportions of c9- and c11-18:1 isomers in total c-18:1 followed by SCF from steers fed SS, PRF from steers fed FS and SS had the lowest proportions (P \ 0.05). The proportions of c12-18:1 were greatest in PRF from steers fed SS, SCF from steers fed FS had the lowest proportions, SCF from steers fed SS and PRF from steers fed FS had intermediate proportions (P \ 0.05). Proportions of t11-18:1, the major t-18:1 isomer accounted for about 45–50 % of total t-18:1 isomers across all treatments (Fig. 2b). The proportions of t-18:1 isomers were significantly influenced (P \ 0.05) by both types of oilseed and adipose tissue (Fig. 2b). Proportions of t-18:1 isomers with double bonds from carbon 6 to 12 were greater (P \ 0.05) when feeding SS while those with double bonds from carbon 13 to 16 were greater (P \ 0.05) when feeding FS. All the t-18:1 isomers were influenced by adipose tissue
type, with PRF as opposed to SCF having slightly greater (P \ 0.05) proportions of individual t-18:1 isomers. Relationships Among PUFA-BHP in the Adipose Tissues In the current study, the relationships among PUFA-BHP and their interrelationships with oilseed and tissue samples were explored by PCA (Fig. 3). The PCA loading plot of the first two principal components explained 99 % (PC-1, 96 %; PC-2, 3 %) of the total variation in the composition of PUFA-BHP (Fig. 3a). The loading plot (Fig. 3a) was characterised by three distinct clusters of PUFA-BHP. The first cluster extending from the upper-right quadrant to the lower-right quadrant was mainly comprised of AD and CLA isomers with the first double bond at carbon 8 or 9 from the carboxyl end. The CLA isomers with the first double bond at carbon 10 and t-18:1 isomers with double bonds from carbon 6 to 12 were situated on the upper-left
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Lipids (2014) 49:275–286
A 82
% of total cis-MUFA
80 78 76
a
b
c c
74 72 70 68 66 64 62 12 a
10 8 6 4 2
a
b c
0 c9
c11
c
c
b b a b c c12
a c
a b c
c13
c
c14
c d c15
b
c
c
a b
c16
% of total trans-18:1 isomers
B 48 44 40 36 32 28 24 20 16 12 8 4 0 t6/t7t/8 t9 Subcutaneous fat-Flaxseed
t10 t11 Subcutaneous fat-Sunflower-seed
t12 t13/t14 Perirenal fat-Flaxseed
t15 t16 Perirenal fat-Sunflower-seed
Fig. 2 Effects of types of oilseed and adipose tissue on cis-18:1 (a) and trans-18:1 (b) isomers from yearling steers fed grass hay based diets. Means with different letters (a–d) for a particular
biohydrogenation product are significantly different (P \ 0.05); a significant oilseed effect (P \ 0.05); b significant tissue effect (P \ 0.05)
quadrant and constituted the second cluster. The third cluster stretching from the lower-left quadrant to the lowerright quadrant was made up of CLNA isomers (c9t11c15-; c9t11t15-18:3), AD and CLA isomers with the first double bond in position 11 or 12 from the carboxyl end. The PCA loading plot (Fig. 3a) also showed that t6/t7/t8-18:1 and t7,c9-CLA; t9-18:1 and t9,c11-CLA; t11-18:1 and c9,t11CLA; t12-18:1 and c9,t12-18:2; t13-18:1 and t9,t12/c9t1318:2 were located on opposite sides. The PCA score plot of samples from animals fed oilseeds (Fig. 3b) indicated that samples from SS fed steers were mainly located on the upper quadrants associated with AD and CLA isomers with the first double bond at carbon 8 or 9 from the carboxyl end and t-18:1 isomers with double bonds from carbon 6 to 12. However, some AD isomers (t8,c13-; c9,c15- and t9,t12-/c9t13-18:2) and c-18:1 isomers (c9-; c11-18:1) were located close to the border associated with both SS and FS feeding. In the same score plot (Fig. 3b), samples from FS fed steers were mainly situated in the lower quadrants associated with CLNA
isomers, AD and CLA isomers with the first double bond in position 11 or 12 from the carboxyl end and t-18:1 isomers with double bonds from carbon 13 to 16. In the PCA score plot of tissue samples (Fig. 3c), the SCF samples were concentrated in the lower- and upperright quadrants associated with AD and CLA isomers with the first double bond in positions 7 to 9 from the carboxyl end. The PRF samples were found in lower and upper-left quadrants (Fig. 3c) associated with c9,t11,c15-18:3, AD and CLA isomers with the first double bond in position 11 or 12 from the carboxyl end CLA isomers with the first double bond on carbon 10, and t-18:1 isomers.
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Discussion The observation that feeding a FS containing (ALA-rich) diet, and PRF had greater proportions of c9,t11,c15-18:3, the major CLNA isomer, were supported visually by similar PCA associations. The enrichment of c9,t11,c15-
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281
Fig. 3 Projection of polyunsaturated fatty acid biohydrogenation products (a), and samples in relation to types of oilseed (b) and adipose tissue (c) in the plane defined by two principal components
18:3 in adipose tissues when feeding FS was reported earlier [9, 10, 20]. Current findings, therefore, confirm that CLNA metabolism in the rumen is related to ALA. In fact, ALA is initially isomerised to c9,t11,c15-18:3 during biohydrogenation in the rumen [21–23]. The reasons for the observed differences in the proportions CLNA isomers between PRF and SCF are, however, not clear. Overall, high proportions of a given FA in the tissues could reflect selective uptake or concentration in different lipid classes (e.g. phospholipids vs. neutral lipids), whereas low proportions might indicate a selective discrimination process or a greater rate of metabolism of a given FA [24]. Martı´nez Marı´n et al. [25] suggested that c9,t11,c15-18:3 may be more derived from diet whereas c9,t11,t15-18:3 maybe be more a product of desaturation of t11,t15-18:2 which is consistent with our PCA where c9,t11,t15-18:3 is more closely associated with a tissue with higher D9 desaturase activity (i.e., SCF). Given that cell culture and animal model studies have demonstrated that plant-derived CLNA isomers including c9,t11,c15-18:3 possess anti-
inflammatory, immune-modulatory, anti-obesity and anticarcinogenic properties [26, 27], processed beef products made with PRF from steers fed FS containing diets could be a richer source of CLNA in human diets, but contents would likely have to be increased considerably to promote any beneficial biological activity. The analysis of variance (ANOVA) output showing AD isomers with the first double bond in position 11 or 12 from the carboxyl end were greater in PRF and when feeding the FS diets, and were associated with FS feeding and PRF in PCA loading plots, is in line with our previous reports when feeding FS containing diets [9, 10]. In general, the observed dissimilarities in the proportions of AD isomers could be a consequence of differences in rumen metabolism between FS and SS [20], and tissue-specific differences in incorporation of individual FA [28]. It is likely that groups of FA located close together (clustered) in a PCA loading plot have the same origin and/or may have common ruminal biohydrogenation pathways [29–31]. Current findings are consistent with known rumen biohydrogenation pathways where ALA yields CLNA isomers, chiefly c9,t11,c15-18:3,
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which are in turn sequentially hydrogenated to yield AD isomers, chiefly t11,c15-18:2 through the activities of isomerase and reductase enzymes, respectively [21, 22]. The present results further suggest that AD isomers with the first double bond at carbon 11 or 12 are preferentially deposited in PRF and may have shared metabolic pathways in the adipose tissues. If AD isomers derived from ALA are found to have beneficial effects on human health, inclusion of PRF trim fat from steers fed diets containing FS in processed beef products would offer the potential to substantially increase their consumption by humans. The findings that feeding SS vs. FS and SCF vs. PRF had greater proportions of AD isomers with the first double bond at carbon 8 or 9, and that these AD isomers were located close together and associated with SS supplementation and SCF in PCA loading and score plots, agrees with previous reports when feeding diets containing SS [20, 32], and provides additional support for the biohydrogenation pathways of LA. Indications from PCA that t8,c13-; t9,c12-; c9,c15- and t9,t12-/ c9t13-18:2 were associated with both SS and FS feeding suggest that they are found in common biohydrogenation pathways for LA and ALA. Present results also suggest that AD isomers derived from LA are preferentially incorporated in SCF and may share common metabolic routes in adipose tissues. In the event that LA-derived AD are found to have positive human health effects, using subcutaneous trim fat to produce beef products enriched with these isomers would increase their intake by consumers, and amounts could be likely be increased by feeding steers forage-based diets supplemented with SS. The ANOVA output showing that PRF from steers fed FS had the greatest proportions of CLA isomers with the first double bond in position 11 or 12 from the carboxyl end, and PCA output indicating that these CLA isomers were grouped together and associated with FS feeding and PRF, suggest that these isomers are more closely related to ruminal biohydrogenation of ALA than LA as previously reported [23, 33, 34]. In fact, the current results show that c9,t11,c15-18:3, AD and CLA isomers with the first double bond in position 11 or 12 were all increased by feeding diets containing FS, were preferentially deposited in PRF, and were grouped together in the PCA loading plot suggesting that they have the same origin or have common biohydrogenation pathways in the rumen. In support of our findings, Hino and Fukuda [35] presented data from two Butyrivibrio fibrisolvens strains suggesting t11,c13-CLA is formed by isomerisation of t11,c15-18:2, the major AD isomer. This major AD isomer is derived from c9,t11,c1518:3, the main product of ALA isomerisation [29–31]. The c/t11,c/t13-18:2 isomers are linked together in the well-established biohydrogenation pathway of ALA [21,
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23, 34]. The CLA isomers with the first double bond at carbon 12 have been associated with feeding ALA-rich diets [10, 20, 32] although no putative pathways for their occurrence have been proposed. The ANOVA output showing that SCF from steers fed SS had the largest proportions of t7,c9-; t8,c10-; t9,c11and c9,t11-18:2, whereas PRF from steers fed SS had the greatest proportions of t9,t11-; t10,c12- and t10,t12-18:2, combined with PCA output indicating that these two groups of isomers were respectively associated with SCF and PRF but jointly associated with SS feeding, suggest that these CLA isomers were likely produced by microbial isomerisation of LA in the rumen as reported earlier [23, 33]. In support of the current results, supplementation of ruminant diets with LA-rich sources have been demonstrated to increase the proportions of CLA isomers with the first double bond from carbon 7 to 10 in animal products when compared to supplementation with ALA-rich sources [20, 32]. This is also consistent with previously reported pathways where LA biohydrogenation leads mostly through CLA vs. AD, whereas ALA biohydrogenation leads mostly through AD [9, 36]. The observed tissuespecific differences between CLA isomers with the first double bond from carbon 7 to 9 and those with the first double bond at carbon 10 may be because these two groups of isomers are produced by different bacterial species (i.e., Propionibacterium species vs. B. fibrisolvens) that have different optimal ruminal pH ranges [21, 37] and/or are metabolised differently in the mammalian cells [38, 39]. The observation that SCF had greater proportions of c9,t11-18:2 than PRF concurs with previous findings [10, 13] indicating that SCF may have greater D9 desaturase catalytic activity index than PRF [13]. These findings suggest that SCF as opposed to PRF is a better source of rumenic acid in beef cattle. If rumenic acid-enriched beef products are to be produced, SCF from steers fed LA-rich diets might, therefore, be a better source of trim fat than PRF from steers fed ALA-rich diets. The emphasis to enrich beef with c9,t11-18:2 relates to its purported potential to prevent carcinogenesis and atherosclerosis, and modulate immune and inflammatory responses in animal models [4, 40]. In addition, a significant reduction in inflammatory parameters such as interleukin-6, interleukin-8 and tumour necrosis factor-alpha, and in the extent of platelet aggregation was found in humans consuming 0.145 g/day of c9,t11-18:2 from naturally enriched Pecorino cheese [41]. In the current study, the estimated levels of c9,t11-18:2 in regular ground beef (70 % lean ? 30 % fat) made with SCF from steers fed diets containing FS and SS would be 0.42 and 0.56 g per 100 g of tissue, which would account for 14 and 19 % of the estimated dietary CLA intake of 3.0 g/day considered necessary for cancer prevention [42]. On the contrary, regular ground beef made with PRF from
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steers fed diets containing FS and SS would be 0.24 and 0.30 g per 100 g of tissue, which would contribute 8 and 10 % of the estimated dietary CLA intake considered necessary for cancer prevention [42]. These findings imply that ground beef products made with SCF from steers fed LArich diets may be better sources of c9,t11-18:2 than ground beef made with PRF from steers fed ALA-rich diets. Trans10,cis-12-CLA has also been reported to exhibit other positive effects including reducing body fat gain while enhancing lean body mass gain [4, 39] and inhibiting atherosclerotic lesion development [43] but has been demonstrated to have detrimental effects in animal models [40, 44]. Overall, rumenic acid appears to promote greater health benefit, with less risk than the t10,c12-CLA isomer and is found in larger proportions in beef tissues. The human health effects of most other CLA isomers have, however, not been elucidated and merit investigation as suggested by Mapiye et al. [10] and Nassu et al. [9]. The ANOVA and PCA findings that c-18:1 isomers with the first double bond from carbon 15 to 16 were enriched by FS feeding, largely incorporated into PRF, and clustered together with other isomers likely largely derived from ALA, indicates that they likely originated from ALA as previously suggested [23, 32]. The observation that several minor c-18:1 isomers were elevated by feeding FS containing diets suggests that ALA is more extensively biohydrogenated in the rumen, and yields a greater diversity of isomers compared to LA [45]. The disparities between PRF and SCF in the composition of these c-18:1 isomers, likely largely derived from ALA, relates to their differences in incorporation of specific FA [24, 28]. The slight differences in the proportions of some c-18:1 isomers (c9-; c11-18:1) observed when feeding oilseeds and the PCA results indicating these isomers were associated with both FS and SS feeding could mean that these isomers have ALA and LA as their precursors. The ANOVA output showing that t18:1 isomers with double bonds from carbon 6 to 12 were mainly increased when feeding diets containing SS while those with double bonds from carbon 13 to 16 were elevated when feeding diets containing FS agree with PCA output showing that these two groups of isomers had distinct clusters associated with SS and FS feeding. Bessa et al. [32] and Loor et al. [48] made similar observations when feeding LA- and ALA-rich diets. This likely stems from LA and ALA being specific precursors for these two groups of t-18:1 isomers [21, 23, 33]. In support of the ANOVA output showing that PRF had greater proportions of t-18:1 isomers, PCA output also illustrated these isomers were associated with PRF. Similar to current results, Jiang et al. [13] and Mapiye et al. [10] reported that PRF exhibited higher proportions of total t-18:1 and t11-18:1 than SCF. This may be related to a lower D9 desaturase index in PRF compared to SCF as
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found by Jiang et al. [13], which may be associated with an age-related decline in kidney’s adipose tissue capacity to desaturate FA. The interest in raising the proportions of t11-18:1 in beef is linked to its potential to reduce pro-inflammatory cytokines [41, 49] and platelet aggregation in humans [41], and substantially reduce plasma triglycerides in animal models [50]. In addition, t11-18:1 may potentially benefit human health through its D9 desaturation to c9,t11-18:2, which seems to have additional positive effects on human health [4, 40]. In the current study, the estimated levels of t1118:1 in regular ground beef made with PRF from FS and SS steers would be 1.45 and 2.02 g per 100 g of tissue whereas regular ground beef made with SCF from FS and SS steers would be 0.81 and 1.09 g per 100 g of tissue. Despite that the levels of t11-18:1 considered beneficial to human health are not yet known, it has been reported up to 30 % of t11-18:1 is desaturated to c9,t11-18:2 in humans [51] suggesting that t11-18:1 could be considered as potential c9,t11-18:2. The estimated potential c9,t11-18:2 from VA bioconversion in PRF from FS and SS steers would, therefore, contribute about 15 and 20 % of the dietary CLA intake considered necessary for cancer prevention [42] compared to SCF from FS and SS steers, which would contribute 8 and 11 %, respectively. Current findings suggest that PRF from steers fed SS may be more useful in producing ground beef products with relatively high proportions of t11-18:1 (potential c9,t11-18:2) compared to SCF from steers fed FS. Trans-18:1 isomers other than t11-18:1 have been associated with unhealthy changes in blood lipid profiles in animal models [52, 53] but the effects of many individual isomers on human health have not been investigated. It is important to note that several ruminant studies found relatively higher proportions of t-18:1 isomers, chiefly t11-18:1 in internal fat depots (e.g. PRF and omental fat) and relatively higher proportions of CLA, chiefly c9,t11-18:2 in external depots (SCF and seam fat) [13, 54, 55]. In this regard, it may be important to determine changes in the proportions of PUFA-BHP in response to oilseeds between fat depots with the same anatomical position and their relationships. Overall, the differences in the proportions and of PUFA-BHP and their relationships observed in the current study could be of importance in formulating value-added processed beef products and in determining their safety and human health effects. In PCA loading plots, variables located opposite to each other are negatively correlated and may be biosynthetically related [31]. For example, the higher proportions of t1118:1 in PRF as depicted in Fig. 3a and conversely indicates lower amounts in SCF, and lower amounts of t11-18:1 in SCF are then negatively correlated with the higher amounts of c9,t11-18:2 found in SCF. Overall, current findings,
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therefore, give further indication that t7-18:1 and t7,c918:2; t9-18:1 and t9,c11-18:2; t11-18:1 and c9,t11-18:2; t12-18:1 and c9,t12-18:2; t13-18:1 and c9,t13-18:2 were inversely related providing further support for the D9 desaturation of these t-18:1 isomers to their corresponding c/t dienoic acids in animal tissues as previously reported [21, 22, 48]. However, it is difficult to separate t6-, t7-, and t8-18:1; t13- and t14-18:1 and t9,t12-18:2 and c9t13-18:2 analytically, which precluded quantitation of t7-18:1 and t13-18:1 and their conversion to t7,c9-CLA and c9,t1318:2, respectively. Given that when rumen pH decreases, ruminal biohydrogenation of LA may shift to a pathway involving t10,c12-CLA formation and its reduction to t1018:1 [56], and de novo synthesis of t10,c12-CLA from the t10-18:1 in mammalian tissues is not possible due to the lack of D12 desaturase, clustering of t10-18:1 with t10,c12 and their association with LA-rich diets was expected.
Conclusions The present study provided evidence for a number of novel oilseed by fat depot interactions on adipose tissue fatty acid composition. The BHP likely largely derived from LA such as AD and CLA isomers with the first double bond at carbons 7–9 from the carboxyl end, and t-18:1 isomers with double bond from carbon 6 to 12 increased in proportion with SS feeding, and were found in larger proportions in SCF. On the other hand, BHP likely largely derived from ALA including CLNA isomers, AD and CLA isomers with the first double bond on carbon 11 or 12, c-18:1 isomers with double bonds from carbon 15 to 16 and t-18:1 isomers with double bonds from carbon 13 to 16 were elevated when feeding FS and were found in proportions in the PRF. The PCA results revealed similar oilseed and adipose tissue type patterns for BHP derived from LA and/or ALA providing some indication of their unique relationships and points where they may overlap. The current study outlines opportunities to select diets and adipose tissue sources to enrich a number of PUFA-BHP with positive human health potential (i.e., t11-18:1, c9,t11-18:2 and c9,t11,c15-18:3). In addition, a number of other BHP can be differentially enriched based on diet and tissue and this will assist in their isolation and evaluation of their health effects, investigation of their origin and fate, and development of feeding and harvest strategies to further promote their accumulation or depletion. Acknowledgments Alberta Livestock and Meat Agency (ALMA) is acknowledged for funding this research. Drs C. Mapiye and T. D. Turner received NSERC Fellowships funded through ALMA.
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