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Effect of dietary soybean oil and antioxidants on fatty acids and volatile compounds of tail subcutaneous and perirenal fat tissues in fattening lambs

Effect of dietary soybean oil and antioxidants on fatty acids and volatile compounds of tail... Background: Fat is the primary source of the volatiles that determine the characteristic flavors of animal products. Because unsaturated fatty acids (UFAs) contribute to changes in flavor as a result of the oxidation process, a feeding trial was performed to investigate the effects of dietary soybean oil or antioxidants on the fatty acid and volatile profiles of the tail subcutaneous (SF) and perirenal fat tissues (PF) of fattening lambs. Thirty-six Huzhou lambs were assigned to four dietary treatments in a randomized block design. The lambs’ diets were supplemented with soybean oil (0 or 3 % of DM) or antioxidants (0 or 0.025 % of DM). Results: Neither soybean oil nor antioxidant supplementation had an effect on lamb growth (P > 0.05). In regard to tail SF, soybean oil supplementation increased the 18:2n6t (P < 0.05) and the total amount of volatile acids, whereas antioxidant supplementation increased the content of C18:2n6c and C18:3n3 (P < 0.05) but had no effect on the volatiles profile. In regard to PF, dietary soybean oil supplementation increased the C18:0 content (P <0.01); decreased the C18:1 (P = 0.01), C22:1 n9 (P < 0.01) and total UFA (P = 0.03) contents; and tended to decrease the E-2- octenal (P = 0.08), E, E-2, 4-decadienal (P =0.10), 2-undecenal (P = 0.14) and ethyl 9-decenoate (P = 0.10) contents. Antioxidant supplementation did not affect either the fatty acid content or the volatiles profile in the PF. Conclusions: Tail SF and PF responded to dietary soybean oil and antioxidant supplementation in different ways. For SF, both soybean oil and antioxidant supplementation increased the levels of unsaturated fatty acids but triggered only a slight change in volatiles. For PF, soybean oil supplementation decreased the levels of unsaturated fatty acids and oxidative volatiles, but supplementation with antioxidants had little effect on PF fatty acids and the volatiles profile. Keywords: Aldehydes, Flavor, Oxidation, Unsaturated fatty acids Background increased C18:2 and C18:3 levels in lamb and goat meat in The isomerization and hydrolysis effects of ruminal response to soybean oil supplementation [4, 5]. At the microbial enzymes result in ruminant-derived products same time, however, higher levels of PUFAs in animal containing higher n-3 polyunsaturated fatty acids (PUFA) products may alter the flavor of the meat. Study results and conjugated linoleic acids, which have been shown to have been inconclusive and often contradictory, with some benefit human health. Thus, dietary supplementation with researchers suggesting that higher PUFA concentrations PUFA-rich vegetable oil, fish oil or oil seeds is an effective in muscle tissues might result in reduced meat quality strategy for increasing PUFA levels in meat or milk prod- [6, 7], whereas others have noted that higher proportions ucts [1–3]; for instance, several studies have reported of C18:3 n3 in lamb phospholipids are associated with reductions in abnormalities in lamb flavor [8]. Because * Correspondence: jiakunwang@zju.edu.cn PUFAs are very sensitive to oxidization, the inconsistent Laboratory of Ruminant Nutrition, College of Animal Sciences, Zhejiang results could be attributed to the various intermediate University, 866 Yuhangtang Road, Hangzhou, 310058 Zhejiang, P. R. China products of oxidation of different PUFAs [9], such as Full list of author information is available at the end of the article © 2016 Peng et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Peng et al. Journal of Animal Science and Biotechnology (2016) 7:24 Page 2 of 9 E,E-2,4-decadienal, an oxidant product of linoleic acid Table 1 Ingredients and chemical composition of the diet (%, DM basis) (C18:2) and the source of “oil” aroma, which contributes to the change in flavor of the cooked meat of lambs whose Items Diets c d e f diet was supplemented with sunflower oil [10]. Many C A O AO studies have focused on protecting PUFAs from oxidation Ingredients, % as DM basis through the use of antioxidants, and several synthetic Peanut vine 50.0 50.0 50.0 50.0 antioxidants, such as butylated hydroxy anisole (BHA), Corn 23.7 23.7 0.0 0.0 butylated hydroxy toluene (BHT) and alpha tocopherol Wheat bran 2.8 2.8 28.4 28.4 have been successfully employed to prevent or restrict Rapeseed cake 8.3 8.3 3.4 3.4 lipid oxidation in meat products [11]. Fat tissues are the source of many valuable products in Tofu dreg 13.1 13.1 13.1 13.1 the food industry. For example, sheep store excess fat in Soybean oil 0.0 0.0 3.0 3.0 their tails during times of abundant food, and this tail fat Antioxidant 0.0 0.025 0.0 0.025 is used to produce ghee, a type of clarified butter [12]. Salt 0.8 0.8 0.8 0.8 Perirenal fat along with the triceps brachii muscles can CaHPO 0.5 0.5 0.5 0.5 be used to produce hamburger meat [13]. Given that the NaHCO 0.3 0.3 0.3 0.3 generation of flavor volatiles is highly dependent on the 3 cooking method, most studies have focused on the flavor Premix 0.5 0.5 0.5 0.5 development of cooked meat, but there is scant informa- Chemical composition tion about raw meat. The fatty acids and volatiles in raw DM, % 79.8 79.8 80.4 80.4 animal tissues could be considered as the basal compo- DE, MJ/kg 12.9 12.9 13.0 13.0 nents that play a part in the complex reactions between CP, % of DM 15.4 15.4 15.3 15.3 fatty acids and other non-volatiles during cooking; it is Ca, % of DM 1.6 1.6 1.5 1.5 therefore desirable to identify the fatty acids and vola- tiles in fat tissue, as the solvents of volatiles. Because the P, % of DM 0.4 0.4 0.5 0.5 effect of dietary soybean oil supplementation on the Diet was formulated to meet the Feeding Standards of Meat-producing Sheep and Goats (Ministry of Agriculture of P.R. China, 2004) volatiles profile in the raw tissue of lambs is limited, we Diets included four treatments (C, A, O and OA) and are the same as in hypothesized that dietary soybean oil supplementation Tables 2, 3, 4, 5, 6 and Fig. 1 C is the control group; the diet did not contain antioxidants or soybean oil (3 % DM) might increase the level of PUFAs in tail sub- A is the antioxidant group; the diet consisted of the control diet plus cutaneous and perirenal fat tissues of fattening lambs, antioxidant (0.025 % of DM) with coinciding antioxidant supplementation to minimize O is the soybean oil group; the diet consisted of the control diet plus soybean oil (3 % of DM), and the dietary energy and protein levels were PUFA oxidation in fat tissues. adjusted to match those of the control diet Huzhou sheep, renowned for their rapid growth rates OA is the soybean oil plus antioxidant group; the diet consisted of the soybean oil diet plus antioxidant (0.025 % of DM) and high fertility, are among the most common breed of Formulated to provide (per kilogram of DM) 1 200 000 IU of vitamin A, 280 sheep raised in China. Here, we examined the effects of 000 IU of vitamin D, 5 000 mg of vitamin E, 14 000 mg of Zn, 3 500 mg of Mn, dietary supplementation with a UFA (soybean oil) and 3 000 mg of Cu, 200 mg of I, 60 mg of Co and 100 mg of Se antioxidants on the fatty acid and volatiles profile of the tail SF and PF of fattening Huzhou lambs. Plus, a proprietary blend of antioxidants that includes ethoxyquin and silicon dioxide; Novus International Inc., Methods St. Charles, MO, USA), designated as the Antioxidant Animals and management group (A); 3) basal diet supplemented with soybean oil The experimental procedures used here, including the (3 % DM), designated as the Oil group (O); and 4) basal feeding, transport and slaughter of the subject sheep, diet supplemented with both soybean oil and antioxidants, were approved by the Zhejiang University Experimental designated as the Oil and Antioxidant group (OA). All Animal Welfare Ethics Committee. groups were fed equal portions twice daily at 0830 and Thirty-six 7-month-old male Huzhou male lambs 1630 h, and the lambs were given free access to drinking (29.9 kg ± 2.2 kg [mean ± SD]) were randomly divided into water. Feeding trials were conducted for a period of four groups based on a randomized block design, with 7 wks, consisting of 1 wk for adaptation followed by 6 wks each group composed of three units of three lambs. Four of treatment. Feed intake and residual food amounts were dietary treatments (concentrate:forage ratio of 5:5) catego- recorded throughout the testing period. rized by soybean oil and antioxidant as the main effects (Tables 1 and 2) were used, with treatments consisting of Sample collection 1) basal diet without supplementation (C); 2) basal diet At the end of the experiment, all lambs were weighed supplemented with antioxidants (0.025 % DM of Agrado prior to the morning feeding for two consecutive days Peng et al. Journal of Animal Science and Biotechnology (2016) 7:24 Page 3 of 9 Table 2 Fatty acid composition of the diet (percentage of total 1 mL of the upper layer was transferred to a new tube fatty acids) and dried by nitrogen. The FAMEs were dissolved in Fatty acids, % C/A O/OA 0.9 mL of hexane and 0.1 mL of methyl heneicosanoate (1 mg/mL) and then transferred to clean vials prior to C10:0 0.04 0.01 GC analysis. C12:0 0.34 0.19 A GC 6890 N with an FID detector (Agilent Technolo- C14:0 0.32 0.20 gies Inc., CA, USA) equipped with a DB-23 column (30 m C15:0 0.03 0.02 long, 0.25 mm ID, 0.25-μm film) (Agilent Technologies C16:0 8.26 7.93 Inc., CA, USA) was used to analyze the fatty acid profiles C16:1 0.17 0.11 of the samples at injector and detector temperatures of 220 °C and 260 °C, respectively. The temperature program C17:0 0.12 0.10 consisted of an initial temperature of 70 °C, an increase at C18:0 3.39 3.15 a rate of 58 °C/min to 240 °C and a final temperature of C18:1 n9c 14.26 11.38 240 °C for 5 min. Fatty acids were identified by compari- C18:2 n6t 0.20 0.35 son to known external standard mixes of 37 FAMEs C18:2 n6c 17.64 22.23 (Sigma Aldrich, China). Methyl-heneicosanoate was se- C18:3 n3 2.48 2.81 lected as the internal standard, with the quantity of each fatty acid calculated according to the relative peak area of C20:1 0.72 0.31 the internal standard. C20:5 n3 0.13 0.07 C22:1 n9 1.68 0.86 Volatile compounds analysis C23:0 0.06 0.12 Headspace solid phase micro-extraction (SPME) coupled C24:0 0.04 0.06 with gas chromatography-mass spectrometry (GC-MS) was C22:6 n3 0.02 0.01 used to analyze the volatiles content of fat tissue, as de- scribed elsewhere [15]. Briefly, SPME with 50/30 mm divi- C24:1 n9t 0.10 0.10 nylbenzene/carboxen/polydimethylsiloxane fiber was used Saturated 12.60 11.77 to extract the volatiles from 1-g samples of fat tissues at Unsaturated 37.40 38.23 120 °C. A DB-5 capillary column (30 m × 0.25 mm × 0.25 mm) (Agilent Technologies Inc., CA, USA) was used and transported to a slaughterhouse after being fasted to analyze the volatiles. After desorption of SPME at 250 °C for 24 h. The total PF and right side of the tail fat were for 5 min, volatiles were separated under the following sliced following removal of the vessels and connective chromatographic conditions: GC oven temperatures were tissues, and approximately 20 g of the PF and tail SF increased from 40 to 250 °C at a rate of 38 °C/min and then were subsampled and vacuum-packed after slaughter. held at 250 °C for 5 min, with helium used as the carrier The samples were stored at 4 °C for 24 h, followed by gas at a flow rate of 0.8 mL/min. The electron impact en- storage at −80 °C for the subsequent determination of ergy was set at 70 eV, and data were collected in the range volatiles and fatty acids. of m/z 40–650. The Wiley library and mass spectral data- base (NIST 2002, Washington, DC, USA) coupled to the Fatty acids analysis Kovats retention indices taken from a series of standards Fatty acid methyl esters (FAMEs) were produced from (C6-C25 n-alkanes) were used to identify the mass spectra 20 mg of fat samples via the one-step trans-esterification of the volatile compounds. method, in accordance with the procedures described by Rule [14]. The FAMEs were dissolved in 0.9 mL of hex- Statistical analysis ane and 0.1 mL of methyl heneicosanoate as an internal Growth performance, fatty acid content and volatiles pro- standard (1 mg/mL) and then transferred to clean vials file data were analyzed using the GLM procedure of the for gas chromatography (GC) analysis according to the SAS software system (version 9.1). The model included procedures described in a previous study [15]. In brief, soybean oil, antioxidants and the interaction between soy- 20-mg fat samples were placed in 10-mL screw-capped bean oil and antioxidants. The means were compared tubes, to which 1 mL each of a boron trifluoride metha- when the interaction terms of the model were significant nol solution and methanol were added. The tubes were (P < 0.05) using the LAMEANS and PDIFF separation of then placed in an 80 °C water bath for 2 h and vortexed the entire group. Discriminant function analysis (DFA) every 5 min. After the tubes had cooled, 1.5 mL of hex- was performed to distinguish the characteristics of the ane and 1.5 mL of double distilled water were added and volatiles among the four groups. All data were normalized thoroughly mixed. Upon cooling to room temperature, with a log10 transformation prior to DFA. Peng et al. Journal of Animal Science and Biotechnology (2016) 7:24 Page 4 of 9 Results As shown in Table 5, dietary soybean oil supplemen- Growth performance tation increased the content of total acids (P = 0.03) As shown in Table 3, no significant effect of soybean oil and decreased the contents of methyl 2,8-dimethylde- and antioxidant on growth performance was detected, but canoate, 2-hexyl-1-decanol and 2-pentadecanone in SF final body weight (P = 0.13) and average daily gain (ADG) (P < 0.05); moreover, soybean oil supplementation led (P = 0.08) were slightly reduced in sheep undergoing the to slightly decreased E-2-nonenal (P = 0.11) levels, and soybean oil treatment. Antioxidant supplementation tended increased ethyl caprinate, decanoic acid and undecanoic to decrease dry matter intake (DMI) (P = 0.10), final body acid (0.05 < P < 0.20) levels. No volatile compounds were weight (P = 0.07) and the ADG of lambs (P =0.07). affected by antioxidant treatment or by the interaction between soybean oil and antioxidant. As shown in Table 6, levels of E-2-octenal, E,E-2,4- Fatty acid profile decadienal, 2-undecenal and ethyl 9-decenoate tended to The primary effects of soybean oil and antioxidant sup- decrease in response to soybean oil supplementation plementation on the fatty acid profiles of SF and PF are (0.05 < P < 0.20), but no volatile compounds were af- shown in Table 4. Palmitic acid (16:0), oleic acid (18:1) fected by the antioxidant treatment. The total content of and stearic acid (18:0) were the three major fatty acids aldehydes was affected by the interaction between soy- in both SF and PF, accounting for more than 85 % of the bean oil and antioxidant supplementation (P = 0.03). total fatty acid content. All of the volatile compounds detected in SF and PF For SF, soybean oil supplementation only increased the were subjected to discriminant function analysis (DFA) content of C18:2 n6t (P = 0.03), whereas antioxidant sup- (Fig. 1). The DFA plot based on the volatiles profile of plementation increased the contents of C17:0 (P = 0.03), SF is shown in Fig. 1a. In DF1 (74.7 %), the C group was C18:3 n3 (P = 0.02) and C18:2 n6c (P = 0.06). No fatty distinguished from the other three groups (A, O and OA acid was affected by the interaction of soybean oil and groups), but those groups were not separated from one antioxidant. another; however, the O group was separated from the For PF, soybean oil supplementation increased the OA group in DF2 (16.1 %). The DFA plot based on the content of C18:0 (P < 0.01) and decreased the propor- volatiles profile of PF is shown in Fig. 1b. In DF1 tion of total UFA (P = 0.03), which was mainly attrib- (66.7 %), the C and CA groups were separated from the uted to decreases in C18:1 (P = 0.01) and C22:1 n9 O and OA groups, but the C group was not distin- contents (P < 0.01). Antioxidant supplementation did guished from the CA group, and the O group was not not affect the fatty acid composition of PF (P > 0.05). separated from the OA group. In DF2 (19.7 %), the C The interaction between soybean oil and antioxidant group was separated from the CA group, and the O significantly affected the total amount of FA (P = 0.03) group was separated from the OA group. and the C22:1n9 content of the PF (P = 0.03). Discussion Volatile compounds profile Growth performance A total of 35 volatile compounds were identified in SF To maintain equal energy and protein levels between the and PF and classified according to their chemical nature control and soybean oil-supplemented diets, a higher as acids, aldehydes, alcohols, esters and others (Tables 5 percentage of wheat bran was used instead of corn in and 6). Aldehydes and esters were the two major types the soybean oil diet, which might increase the satiety of of volatile compounds in both fat tissues, accounting for lambs in groups O and OA and thus reduce their DMI approximately 70 % of the total volatiles detected. and final body weights. Moreover, the effects of dietary Table 3 Effects of supplementation with soybean oil, antioxidant or soybean oil plus antioxidant on growth of fattening lambs Items Diet SEM P-value a b c CA O AO O A O× A Number of lambs 9999 Initial body weight, kg 29.8 30.0 30.0 29.7 0.58 Final body weight, kg 37.5 35.6 35.8 35.1 0.61 0.13 0.07 0.39 Dry matter intake, g/d 1213 1137 1160 1078 42.0 0.22 0.10 0.95 Average daily gain, g/d 188 147 148 141 11.3 0.08 0.07 0.16 The effect of soybean oil, the same as in Tables 4, 5 and 6 The effect of antioxidant, the same as in Tables 4, 5 and 6 The interactive effect of soybean oil and antioxidant, the same as in Tables 4, 5 and 6 Peng et al. Journal of Animal Science and Biotechnology (2016) 7:24 Page 5 of 9 Table 4 Effects of supplementation with soybean oil, antioxidant performance of finishing lambs [16, 17]; on the contrary, or soybean oil plus antioxidant on fatty acid composition of several studies have reported significantly negative effects subcutaneous and perirenal fat tissue in fattening lambs of dietary soybean oil on the growth performances of both Fatty acids, Diet RMSE P-value steers and lambs and suggested that the UFA in the soy- g/100 g FAME CA O AO O A O×A bean oil may impair rumen fermentation and fiber digest- ibility [18, 19]. Potential negative effects of UFAs on Subcutaneous fat tissue b rumen fermentation should therefore be of concern. Total FA 209 211 213 199 44.92 0.79 0.73 0.60 Contrary to what we expected, dietary antioxidant sup- C10:0 0.34 0.34 0.31 0.36 0.15 0.94 0.65 0.64 plementation tended to negatively affect lamb growth. C12:0 0.39 0.32 0.42 0.37 0.15 0.47 0.26 0.88 Agrado Plus is a commercial antioxidant used in feed, and C14:0 4.64 4.15 4.81 4.47 0.88 0.41 0.18 0.81 the results of several studies – including our own previous C14:1 0.81 0.93 0.75 0.95 0.60 0.92 0.44 0.86 research – have demonstrated its beneficial effect on the health and performance of dairy cattle [20, 21]. Here, the C15:0 1.08 1.22 1.08 1.19 0.29 0.87 0.21 0.88 reasons for the negative effects of antioxidant supplemen- C16:0 25.3 24.0 25.8 25.1 2.13 0.29 0.18 0.71 tation on lamb growth were undetermined; it may simply C16:1 2.98 2.60 2.93 2.81 0.97 0.81 0.47 0.69 be due to differences in the physiologies of sheep and C17:0 1.58 1.86 1.46 1.65 0.31 0.13 0.03 0.66 dairy cattle. C18:0 14.8 14.8 13.8 13.3 4.15 0.40 0.86 0.85 C18:1 43.0 44.0 43.2 44.0 2.82 0.90 0.36 0.97 Fatty acid profile Similar to the increased C18:2 in tail SF observed here, diet- C18:2 n6t 0.89 1.00 1.13 1.04 0.18 0.03 0.93 0.11 ary PUFA-rich soybean oil supplementation improved the C18:2 n6c 3.74 4.20 3.75 4.17 0.65 0.97 0.06 0.93 content of C18:2 in the intramuscular fat of goats and C18:3 n6 0.11 0.11 0.13 0.08 0.07 0.94 0.37 0.35 lambs [4, 19]. Because C18:2 is the main fatty acid in soy- C18:3 n3 0.41 0.51 0.40 0.51 0.12 0.90 0.02 0.95 bean oil, the increased proportion of C18:2 in the SF may UFA 66.7 68.1 66.1 66.9 3.05 0.40 0.31 0.76 be due to the dietary C18:2 that was not subjected to U/S 2.03 2.16 1.96 2.05 0.26 0.33 0.24 0.84 biohydrogenation in the rumen. In our previous study of dairy cattle, dietary antioxidants counteracted the negative Perirenal fat tissue b effects of dietary low saturated fats (mainly C18:1) and in- Total FA 145 114 105 119 28.47 0.09 0.41 0.03 creased C18:1 levels in the milk [21], which suggested that C10:0 0.23 0.21 0.20 0.17 0.07 0.16 0.31 0.97 antioxidant supplementation had a positive influence on C12:0 0.31 0.33 0.33 0.42 0.29 0.59 0.62 0.72 UFA accumulation. In this study, however, antioxidant C14:0 3.32 3.11 2.99 2.68 0.64 0.10 0.25 0.82 supplementation increased the concentrations of both C15:0 0.84 0.84 0.86 0.84 0.11 0.89 0.90 0.75 C18:2 and C18:3 in SF regardless of whether it was ingested as part of a normal diet or a diet enriched with C16:0 24.5 23.0 23.9 22.4 2.49 0.53 0.11 1.00 soybean oil, providing a positive signal that the use of anti- C17:0 1.64 1.78 1.51 1.55 0.13 0.00 0.07 0.28 oxidants might improve the nutritional value of Huzhou C18:0 36.2 37.3 39.2 43.3 4.14 0.00 0.09 0.30 lamb tail SF. C18:1 27.4 27.9 25.8 23.6 3.06 0.01 0.42 0.21 Differences between internal (perirenal) and external C18:2 n6c 3.70 3.92 3.82 3.55 1.05 0.73 0.95 0.50 (subcutaneous) fat deposits have been widely demonstrated. C18:3 n6 0.18 0.17 0.18 0.17 0.05 0.88 0.50 0.88 In this study, more UFAs were detected in SF, whereas more SFAs were detected in PF, accounting for 70 % of the C18:3 n3 0.53 0.45 0.48 0.44 0.19 0.62 0.34 0.74 total fatty acids in PF. This finding is consistent with the C20:0 0.52 0.53 0.49 0.58 0.14 0.88 0.28 0.44 higher SFA concentrations previously observed in internal C20:1 0.36 0.28 0.23 0.22 0.15 0.10 0.43 0.52 (kidney) fat compared with external fat depots [22]. As Lee C22:1 n9 0.28 0.21 0.07 0.14 0.09 0.00 0.96 0.03 et al. [23] reported, stearoyl-CoA desaturase (SCD) activity UFA 32.5 32.9 30.6 28.1 4.22 0.03 0.49 0.32 was higher in SF than in PF, which partially explains the U/S 0.48 0.50 0.44 0.40 0.09 0.02 0.57 0.31 higher SFA proportion observed in the PF in this study. RMSE root mean square error, the same as in Tables 5 and 6 The fatty acid profile in PF changed in a different manner The amount of total FA is expressed as mg/g fat tissue than did that of SF in response to dietary supplementation regardless of whether the supplement was soybean oil or soybean oil supplementation on ruminant growth per- antioxidant, similar to observations made by Lee et al. formance were not consistent. Based on our findings [24], who supplemented the diet of lambs with ground both here and in a previous study of Huzhou lambs, soy- whole-fat soybeans. Moreover, Berthelot et al. showed bean oil supplementation did not influence the growth that the differential uptake of FA from the rumen Peng et al. Journal of Animal Science and Biotechnology (2016) 7:24 Page 6 of 9 Table 5 Effects of supplementation with soybean oil, antioxidant or soybean oil plus antioxidant on volatile profiles in subcutaneous fat tissues of fattening lambs a b c Component Abb. RI CSID Diet RMSE P-value C A O AO O A O*A Aldehydes 36.5 36.4 35.0 32.6 14.50 0.61 0.81 0.82 Hexanal Ad1 798 5949 - 0.7 1.9 - - - - E-2-Heptenal Ad2 955 4446437 1.3 1.2 1.1 0.8 1.06 0.41 0.62 0.82 Phenylacetaldehyde Ad3 1040 13876539 2.1 2.1 2.0 1.6 1.35 0.49 0.68 0.64 E-2-Octenal Ad4 1056 4446445 1.6 2.0 1.4 3.4 2.99 0.57 0.29 0.47 Nonanal Ad5 1104 29029 12.1 13.5 14.3 7.2 8.07 0.48 0.33 0.14 E-2-Nonenal Ad6 1157 4446456 12.3 11.1 8.0 8.6 6.45 0.15 0.92 0.70 E,E-2,4-Decadienal Ad7 1295 4446470 4.1 3.4 4.0 4.1 2.26 0.67 0.72 0.60 2-Undecenal Ad8 1368 4446477 3.0 2.5 2.3 7.0 6.46 0.42 0.38 0.27 Esters 34.4 39.1 39.8 42.5 14.36 0.40 0.48 0.84 Ethyl octanoate Es1 1193 7511 1.8 1.1 1.0 4.7 4.35 0.36 0.34 0.16 Methyl decanoate Es2 1328 7759 3.0 1.1 1.3 5.0 5.70 0.59 0.67 0.17 Ethyl cyclohexanepropanoate Es3 1345 55387 5.1 9.8 6.5 5.0 7.00 0.50 0.54 0.22 Methyl 2,8-dimethyldecanoate Es4 1353 487217 3.0 2.9 1.1 1.1 2.17 0.02 0.90 0.96 Ethyl 9-decenoate Es5 1389 455568 3.2 2.0 2.8 1.8 1.91 0.64 0.12 0.89 Ethyl caprinate Es6 1398 7757 2.1 5.0 12.0 7.4 10.33 0.11 0.83 0.31 Methyl 2,4,6-trimethylundecanoate Es7 1487 487035 0.3 0.3 0.5 0.5 0.34 0.14 0.78 0.85 Methyl undecanoate Es8 1490 14847 2.0 2.6 1.5 1.9 1.57 0.28 0.42 0.85 Ethyl 9-oxononanoate Es9 1537 17861 - 3.6 - - - - - Methyl laurate Es10 1554 7847 0.8 0.7 0.7 0.8 0.48 0.81 0.78 0.58 Ethyl laurate Es11 1597 7512 3.3 1.2 1.9 2.4 2.87 0.92 0.43 0.20 Geranyl isovalerate Es12 1606 4515295 0.8 1.3 0.7 0.8 0.79 0.27 0.23 0.51 Methyl 2,6-dimethyltridecanoate Es13 1651 487205 1.1 2.1 2.0 1.6 1.70 0.70 0.67 0.28 Methyl myristate Es14 1769 29024 2.2 1.8 3.5 2.4 2.97 0.38 0.45 0.73 Ethyl myristate Es15 1793 29023 5.6 3.6 4.3 7.1 7.68 0.69 0.89 0.39 Acids 8.1 10.7 12.4 14.7 5.11 0.03 0.20 0.92 (2E)-2-Methyl-2-nonenoic acid Ac1 1269 4724999 1.7 1.4 2.8 2.1 2.20 0.28 0.52 0.79 Decanoic acid Ac2 1355 2863 2.2 3.0 4.5 6.1 4.00 0.07 0.42 0.76 Undecanoic acid Ac3 1465 7888 0.5 0.7 0.8 0.9 0.48 0.15 0.23 0.74 Lauric acid Ac4 1537 3756 - 1.5 1.4 1.7 - - - Tridecylic acid Ac5 1621 12013 0.7 2.0 1.2 0.9 1.49 0.57 0.33 0.17 Alcohols 12.8 9.0 8.9 8.1 6.22 0.29 0.30 0.50 Heptan-1-ol Al1 969 7837 4.0 3.0 3.8 2.7 3.91 0.86 0.47 0.94 1-Octanol Al2 1069 932 1.1 1.1 1.1 1.1 0.96 0.91 0.99 0.89 2-Methyl-1-dodecanol Al3 1492 38544 4.4 2.0 2.2 2.8 3.87 0.62 0.50 0.28 2-Hexyl-1-decanol Al4 1790 86034 3.4 2.9 1.8 1.5 1.78 0.03 0.55 0.96 Others 8.2 4.8 3.8 2.2 3.50 0.01 0.06 0.46 Toluene Ot1 762 1108 3.7 0.9 1.4 - - - - 2-Pentadecanone Ot2 1696 55242 4.7 3.8 2.4 2.1 2.42 0.03 0.48 0.71 All volatile compounds were grouped according to chemical categories. Ad, Ac, Al, Es and Ot are abbreviations for the aldehyde, acid, alcohol, ester and “other” groups, respectively, the same as in Table 6 RI, retention indices of individual compounds relative to C6-C25 n-alkanes, the same as in Table 6 CSID, ChemSpider ID of each chemical (http://www.chemspider.com/), the same as in Table 6 Peng et al. Journal of Animal Science and Biotechnology (2016) 7:24 Page 7 of 9 Table 6 Effects of supplementation with soybean oil, antioxidant or soybean oil plus antioxidant on volatile profiles in perirenal fat tissues of fattening lambs Component Abb. RI CSID Diet RMSE P-value C A O AO O A O*A Aldehydes 34.3 41.4 38.6 31.7 8.65 0.37 0.98 0.03 Hexanal Ad1 798 5949 1.6 - 4.2 2.6 E-2-Heptenal Ad2 955 4446437 2.0 2.2 2.4 1.6 2.02 0.90 0.68 0.53 Phenylacetaldehyde Ad3 1040 13876539 1.6 1.6 6.6 0.3 5.08 0.31 0.09 0.08 E-2-Octenal Ad4 1056 4446445 1.5 1.9 0.5 0.7 1.52 0.08 0.61 0.83 Nonanal Ad5 1104 29029 3.6 4.5 4.8 4.9 2.79 0.45 0.66 0.68 E-2-Nonenal Ad6 1157 4446456 2.1 4.3 2.4 1.9 2.85 0.31 0.42 0.19 E,E-2,4-Decadienal Ad7 1295 4446470 19.5 24.7 16.3 18.1 8.98 0.10 0.29 0.59 2-Undecenal Ad8 1368 4446477 3.0 3.6 1.4 2.3 2.72 0.14 0.46 0.86 Esters 34.8 33.9 34.9 41.9 8.14 0.17 0.31 0.17 Ethyl octanoate Es1 1193 7511 3.6 3.0 4.6 4.2 3.05 0.34 0.68 0.89 Methyl decanoate Es2 1328 7759 10.5 6.1 7.6 10.5 5.74 0.73 0.75 0.10 Ethyl cyclohexanepropanoate Es3 1345 55387 1.8 2.1 1.8 1.5 1.47 0.61 0.92 0.55 Methyl 2,8-dimethyldecanoate Es4 1353 487217 1.5 2.5 1.4 2.3 2.56 0.87 0.32 0.95 Ethyl 9-decenoate Es5 1389 455568 2.1 2.3 1.8 1.2 1.13 0.10 0.63 0.26 Ethyl caprinate Es6 1398 7757 3.4 5.1 2.8 5.4 5.95 0.95 0.31 0.83 Methyl 2,4,6-trimethylundecanoate Es7 1487 487035 0.3 0.6 0.7 1.8 1.10 0.06 0.13 0.33 Methyl undecanoate Es8 1490 14847 2.5 2.7 2.5 3.4 2.68 0.73 0.60 0.72 Ethyl 9-oxononanoate Es9 1537 17861 2.3 - 3.1 6.6 Methyl laurate Es10 1554 7847 0.8 1.0 3.4 1.5 2.21 0.13 0.37 0.27 Ethyl laurate Es11 1597 7512 1.6 2.5 1.1 2.2 1.77 0.56 0.16 0.81 Geranyl isovalerate Es12 1606 4515295 0.7 1.4 0.8 0.8 0.81 0.32 0.23 0.23 Methyl 2,6-dimethyltridecanoate Es13 1651 487205 0.6 0.8 2.2 0.6 1.30 0.20 0.22 0.08 Methyl myristate Es14 1769 29024 1.4 3.0 0.9 1.9 3.10 0.44 0.25 0.76 Ethyl myristate Es15 1793 29023 1.8 3.5 3.0 2.5 3.88 0.94 0.70 0.42 Acids 16.0 12.0 11.1 14.3 11.15 0.74 0.92 0.36 (2E)-2-Methyl-2-nonenoic acid Ac1 1269 4724999 4.1 4.8 3.8 3.5 2.14 0.34 0.81 0.52 Decanoic acid Ac2 1355 2863 - - 1.8 1.5 Undecanoic acid Ac3 1465 7888 9.6 1.9 1.1 3.1 11.71 0.40 0.51 0.25 Tridecylic acid Ac5 1621 12013 3.1 1.7 3.1 1.9 1.94 0.85 0.08 0.93 (7Z)-7-Tetradecenoic acid Ac7 1777 4471826 0.7 1.5 0.9 0.9 0.67 0.41 0.13 0.08 Alcohols 7.9 8.7 10.1 6.8 3.69 0.92 0.35 0.11 Heptan-1-ol Al1 969 7837 1.5 1.2 2.1 0.8 1.12 0.80 0.06 0.26 1-Octanol Al2 1069 932 3.3 3.1 3.0 2.1 1.82 0.40 0.45 0.63 2-Methyl-1-dodecanol Al3 1492 38544 1.8 2.9 3.3 3.4 2.85 0.34 0.54 0.61 2-Hexyl-1-decanol Al4 1790 86034 1.5 2.1 2.5 1.3 2.25 0.96 0.72 0.24 Others 7.0 4.0 5.3 5.5 3.26 0.92 0.23 0.18 Toluene Ot1 762 1108 0.8 1.1 - 1.2 2-Pentadecanone Ot2 1696 55242 6.2 3.3 5.3 4.3 3.37 0.95 0.12 0.42 contributes to variations in trans-fatty acid proportions Volatile compounds profile in the PF, SF and muscles in response to vitamin E Volatile components are not necessarily odor-active. As supplementation [25]. reviewed by Watkins et al., only 15 of 187 volatiles were Peng et al. Journal of Animal Science and Biotechnology (2016) 7:24 Page 8 of 9 Fig. 1 DFA plots of volatile profiles of subcutaneous (a) and perirenal (b) fat tissues from lambs fed normal diets (■, C), diets supplemented with soybean oil (▲, O), diets supplemented with antioxidant (●, A) and diets supplemented with soybean oil plus antioxidant (▼, AO) identified as the primary components of lamb aroma based but its concentration decreased in response to dietary on a gas chromatography − olfactometry (GC-O) analysis, soybean oil supplementation, suggesting that the intensity including the aldehydes E,E-2,4-decadienal, Z-2-nonenal, of “fatty” or “fried”-like flavors of PF was more subdued. E-2-heptenal, methional, E-2-nonenal, decanal, 2,4-E,E- Compared with the effects of soybean oil supplementa- heptadienal, octanal and E-2-octenal [10]. Meanwhile, one tion, antioxidant supplementation triggered fewer changes indicator, termed the odor-activity value, was calculated in both SF and PF. In SF, although antioxidant supplemen- and used to represent the contribution of volatiles to food tation led to higher concentrations of C18:2 and C18:3, flavor [26]. Bueno et al. built a partial least-squares model the fact that we did not detect a simultaneous increase in based on the odor-activity value of 32 volatiles and con- the oxidative by-products (aldehydes) of these UFAs is an cluded that alkenals and alkadienals have negative effects indication that antioxidant supplementation may improve on the intensity of lamb flavor and that E,E-2,4-decadienal anti-oxidative performance and thus hinder the progress and E-2-nonenal were the most abundant volatiles [27]. of UFA oxidation. In the PF, the interaction effect between We found similar patterns in this study: the main alde- soybean oil and antioxidant supplementation on aldehydes hydes in SF (such as nonanal, E-2-nonenal and E,E-2,4- suggested that the presence of the antioxidant slows the decadienal) and those in PF (E,E-2,4-decadienal) largely rate of accumulation of oxidative by-products. Thus, determine the flavor characteristics of SF and PF. although the antioxidant did not induce any direct flavor- When soybean oil was added to the lambs’ diet, the related changes in the composition of the volatiles, it may slight decrease in E-2-nonenal (P = 0.15) observed in the suppress UFA oxidation in fat tissues and thus have an SF was inconsistent with the increase in C18:2, as E-2- indirect positive effect on meat flavor. nonenal is the oxidative product of C18:2, suggesting that To visually represent the different responses of SF and the extent of oxidation in SF might be lower than what we PF to dietary soybean oil and antioxidant supplementa- assumed, but the exact reasons for this phenomenon tion, given the complexity of the factors that determine remain unknown. Moreover, the addition of soybean oil the flavor of fat, the DFA plots of the volatile contents tended to increase the content of the volatile decanoic provide an intuitive outline of the differences between acid (P = 0.07). The odor of decanoic acid is reported to each sample. From Fig. 1a, it can be seen that soybean be positively associated with the oxidation of wine, con- oil supplementation might change the flavor of SF when tributing to the “animal”, “bitterness” and “dairy” charac- no antioxidants are added (74.7 %, C vs O), but less so teristics of wine [28]. Enhanced decanoic acid content when the antioxidant is added (16.1 %, A vs AO); anti- would therefore suggest an increase in SF bitterness as a oxidant supplementation, meanwhile, induced large dif- result of soybean oil supplementation. ferences in the absence of soybean oil (74.7 %, C vs A) In regard to PF, given that the odor threshold of E-2- but did not trigger obvious changes when delivered in octenal is only “4”– that is, the flavor of E-2-octenal conjunction with soybean oil supplementation (16.1 %, O becomes recognizable at concentrations above 4 ng/g vs OA). Thus, the effect of soybean oil supplementation tissue – and despite the content of E-2-octenal decreasing on SF flavor was dependent on whether or not the antioxi- by 1 and 1.2 % with soybean oil supplementation (C vs O: dant was present. As seen in ure 1b, soybean oil supple- 1.5 % vs 0.5 %; A vs AO: 1.9 % vs 0.7 %), the flavor of the mentation led to clear changes when the antioxidant was PF still became less “green, nutty and fatty”,descriptors added (66.7 %, C/CA vs O/OA) and the antioxidant alone that depict the typical flavor of E-2-octenal. Moreover, also altered the volatiles composition (21.9 %, C vs CA, O E,E-2,4-decadienal (with a typical flavor described as “fatty vs OA), but the extent of change caused by the latter sce- and fried foods”) was the primary aldehyde found in PF, nario was less than that of soybean oil supplementation. Peng et al. Journal of Animal Science and Biotechnology (2016) 7:24 Page 9 of 9 We can therefore infer that dietary soybean oil supple- 6. Elmore JS, Cooper SL, Enser M, Mottram DS, Sinclair LA, Wilkinson RG, et al. Dietary manipulation of fatty acid composition in lamb meat and its effect mentation had an effect on PF flavor independent of the on the volatile aroma compounds of grilled lamb. Meat Sci. 2005;69:233–42. presence or absence of the antioxidant. 7. Sañudo C, Enser ME, Campo MM, Nute GR. Maŕ ıa G, Sierra I et al. Fatty acid composition and sensory characteristics of lamb carcasses from Britain and Spain. Meat Sci. 2000;54:339–46. Conclusions 8. Nute GR, Richardson RI, Wood JD, Hughes SI, Wilkinson RG, Cooper SL, et al. In summary, dietary soybean oil supplementation im- Effect of dietary oil source on the flavour and the colour and lipid stability of lamb meat. Meat Sci. 2007;77:547–55. proved the UFA content in tail SF, and antioxidant supple- 9. Scollan ND, Dannenberger D, Nuernberg K, Richardson I, MacKintosh S, mentation further enhanced UFAs by suppressing the Hocquette J-F, et al. Enhancing the nutritional and health value of beef accumulation of oxidative volatiles, thus interacting with lipids and their relationship with meat quality. Meat Sci. 2014;97:384–94. 10. Watkins PJ, Frank D, Singh TK, Young OA, Warner RD. Sheepmeat Flavor and the effect of soybean oil on SF flavor discrimination. Diet- the Effect of Different Feeding Systems: A Review. J Agric Food Chem. 2013; ary soybean oil supplementation induced an decrease in 61:3561–79. the levels of saturated fatty acids and aldehydes in PF. 11. Chastain MF, Huffman DL, Hsieh WH, Cordray JC. Antioxidants in Restructured Beef/Pork Steaks. J Food Sci. 1982;47:1779–82. Antioxidant supplementation, however, had little effect on 12. Kashan NEJ, Azar GHM, Afzalzadeh A, Salehi A. Growth performance and the fatty acid and volatiles composition in the PF. carcass quality of fattening lambs from fat-tailed and tailed sheep breeds. Small Rumin Res. 2005;60:267–71. 13. Turner TD, Aalhus JL, Mapiye C, Rolland DC, Larsen IL, Basarab JA, et al. Abbreviations Effects of diets supplemented with sunflower or flax seeds on quality and ADG: average daily gain; BHA: butylated hydroxy anisole; BHT: butylated fatty acid profile of hamburgers made with perirenal or subcutaneous fat. hydroxy toluene; CLA: conjugated linoleic acid; DFA: discriminant function Meat Sci. 2015;99:123–31. analysis; DMI: dry matter intake; FAMEs: fatty acid methyl esters; GC: gas 14. Rule DC. Direct transesterification of total fatty acids of adipose tissue, and chromatography; GC-MS: gas chromatography-mass spectrometry; GC-O: gas of freeze-dried muscle and liver with boron-trifluoride in methanol. Meat chromatography − olfactometry; PF: perirenal fat tissue; PUFA: polyunsaturated Sci. 1997;46:23–32. fatty acids; SF: subcutaneous fat tissue; SFA: saturated fatty acids; SPME: solid 15. Peng Y-J, Wang J-K, Ren D-X, Lin J, Liu J-X. Different patterns of volatile phase micro-extraction; UFA: unsaturated fatty acid. compounds and fatty acid profiles in the adipose tissues of male and female Hu sheep. Acta Agric Scand Sect A Anim Sci. 2012;62:153–8. Competing interests 16. Berthelot V, Bas P, Pottier E, Normand J. The effect of maternal linseed The authors declare that they have no competing interests. supplementation and/or lamb linseed supplementation on muscle and subcutaneous adipose tissue fatty acid composition of indoor lambs. Meat Authors’ contributions Sci. 2012;90:548–57. YJP carried out the study design, data interpretation and manuscript writing 17. Mao H-L, Wang J-K, Zhou Y-Y, Liu J-X. Effects of addition of tea saponins and editing; JKW was involved in the study design, data interpretation and and soybean oil on methane production, fermentation and microbial manuscript editing; JL was involved in the animal experiment; JXL was involved population in the rumen of growing lambs. Livest Sci. 2010;129:56–62. in the study design, data interpretation and manuscript editing. All authors read 18. Engle TE, Spears JW, Fellner V, Odle J. Effects of soybean oil and dietary and approved the final manuscript. copper on ruminal and tissue lipid metabolism in finishing steers. J Anim Sci. 2000;78:2713–21. 19. Bhatt RS, Soren NM, Tripathi MK, Karim SA. Effects of different levels of coconut Acknowledgments oil supplementation on performance, digestibility, rumen fermentation and This study was financed by the Innovation Team Program of Zhejiang province carcass traits of Malpura lambs. Anim Feed Sci Technol. 2011;164:29–37. (2011R50025). We thank the staff at Changda Sheep Farm for their assistance in 20. He M, Armentano LE. Effect of fatty acid profile in vegetable oils and animal feeding and care. antioxidant supplementation on dairy cattle performance and milk fat depression. J Dairy Sci. 2011;94:2481–91. Author details 21. Wang YM, Wang JH, Wang C, Chen B, Liu JX, Cao H, et al. Effect of different Laboratory of Ruminant Nutrition, College of Animal Sciences, Zhejiang rumen-inert fatty acids supplemented with a dietary antioxidant on performance University, 866 Yuhangtang Road, Hangzhou, 310058 Zhejiang, P. R. China. and antioxidative status of early-lactation cows. J Dairy Sci. 2010;93:3738–45. College of Biological, Chemical Science and Engineering, Jiaxing University, 22. Horcada-Ibáñez A, Beriain-Apesteguía MJ, Lizaso-Tirapu G, Insausti-Barrenetxea 118 Jiahang Road, 314001 Jiaxing, Zhejiang, P. R. China. K, Purroy-Unanua A. Effect of sex and fat depot location on fat composition of Rasa Aragonesa lambs. Agrociencia. 2009;43:803–13. Received: 20 July 2015 Accepted: 28 March 2016 23. Lee J-H, Yamamoto I, Jeong J-S, Nade T, Arai T, Kimura N. Relationship between adipose maturity and fatty acid composition in various adipose tissues of Japanese Black, Holstein and Crossbred (F1) steers. Anim Sci J. 2011;82:689–97. References 24. Lee JH, Waller JC, Melton SL, Saxton AM, Pordesimo LO. Feeding encapsulated 1. Woods VB, Fearon AM. Dietary sources of unsaturated fatty acids for animals ground full-fat soybeans to increase polyunsaturated fat concentrations and and their transfer into meat, milk and eggs: A review. Livest Sci. 2009;126:1–20. effects on flavor volatiles in fresh lamb. J Anim Sci. 2004;82:2734–41. 2. Jerónimo E, Alves SP, Prates JAM, Santos-Silva J, Bessa RJB. Effect of dietary 25. Berthelot V, Broudiscou L, Schmidely P. Effect of vitamin E supplementation replacement of sunflower oil with linseed oil on intramuscular fatty acids of on fatty acid composition of muscle and adipose tissues of indoor lambs lamb meat. Meat Sci. 2009;83:499–505. with special attention on rumen-derived trans monounsaturated fatty acids. 3. Bessa RJB, Lourenço M, Portugal PV, Santos-Silva J. 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Effect of oxygen on volatile and sensory soybean oil supplementation on growth performance, carcass and meat characteristics of cabernet sauvignon during secondary shelf life. J Agric quality and fatty acid composition of intramuscular lipids of lambs. Livest Food Chem. 2011;59:11657–66. Prod Sci. 2004;90:79–88. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Animal Science and Biotechnology Springer Journals

Effect of dietary soybean oil and antioxidants on fatty acids and volatile compounds of tail subcutaneous and perirenal fat tissues in fattening lambs

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Copyright © 2016 by Peng et al.
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Life Sciences; Agriculture; Biotechnology; Food Science; Animal Genetics and Genomics; Animal Physiology
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10.1186/s40104-016-0083-y
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Abstract

Background: Fat is the primary source of the volatiles that determine the characteristic flavors of animal products. Because unsaturated fatty acids (UFAs) contribute to changes in flavor as a result of the oxidation process, a feeding trial was performed to investigate the effects of dietary soybean oil or antioxidants on the fatty acid and volatile profiles of the tail subcutaneous (SF) and perirenal fat tissues (PF) of fattening lambs. Thirty-six Huzhou lambs were assigned to four dietary treatments in a randomized block design. The lambs’ diets were supplemented with soybean oil (0 or 3 % of DM) or antioxidants (0 or 0.025 % of DM). Results: Neither soybean oil nor antioxidant supplementation had an effect on lamb growth (P > 0.05). In regard to tail SF, soybean oil supplementation increased the 18:2n6t (P < 0.05) and the total amount of volatile acids, whereas antioxidant supplementation increased the content of C18:2n6c and C18:3n3 (P < 0.05) but had no effect on the volatiles profile. In regard to PF, dietary soybean oil supplementation increased the C18:0 content (P <0.01); decreased the C18:1 (P = 0.01), C22:1 n9 (P < 0.01) and total UFA (P = 0.03) contents; and tended to decrease the E-2- octenal (P = 0.08), E, E-2, 4-decadienal (P =0.10), 2-undecenal (P = 0.14) and ethyl 9-decenoate (P = 0.10) contents. Antioxidant supplementation did not affect either the fatty acid content or the volatiles profile in the PF. Conclusions: Tail SF and PF responded to dietary soybean oil and antioxidant supplementation in different ways. For SF, both soybean oil and antioxidant supplementation increased the levels of unsaturated fatty acids but triggered only a slight change in volatiles. For PF, soybean oil supplementation decreased the levels of unsaturated fatty acids and oxidative volatiles, but supplementation with antioxidants had little effect on PF fatty acids and the volatiles profile. Keywords: Aldehydes, Flavor, Oxidation, Unsaturated fatty acids Background increased C18:2 and C18:3 levels in lamb and goat meat in The isomerization and hydrolysis effects of ruminal response to soybean oil supplementation [4, 5]. At the microbial enzymes result in ruminant-derived products same time, however, higher levels of PUFAs in animal containing higher n-3 polyunsaturated fatty acids (PUFA) products may alter the flavor of the meat. Study results and conjugated linoleic acids, which have been shown to have been inconclusive and often contradictory, with some benefit human health. Thus, dietary supplementation with researchers suggesting that higher PUFA concentrations PUFA-rich vegetable oil, fish oil or oil seeds is an effective in muscle tissues might result in reduced meat quality strategy for increasing PUFA levels in meat or milk prod- [6, 7], whereas others have noted that higher proportions ucts [1–3]; for instance, several studies have reported of C18:3 n3 in lamb phospholipids are associated with reductions in abnormalities in lamb flavor [8]. Because * Correspondence: jiakunwang@zju.edu.cn PUFAs are very sensitive to oxidization, the inconsistent Laboratory of Ruminant Nutrition, College of Animal Sciences, Zhejiang results could be attributed to the various intermediate University, 866 Yuhangtang Road, Hangzhou, 310058 Zhejiang, P. R. China products of oxidation of different PUFAs [9], such as Full list of author information is available at the end of the article © 2016 Peng et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Peng et al. Journal of Animal Science and Biotechnology (2016) 7:24 Page 2 of 9 E,E-2,4-decadienal, an oxidant product of linoleic acid Table 1 Ingredients and chemical composition of the diet (%, DM basis) (C18:2) and the source of “oil” aroma, which contributes to the change in flavor of the cooked meat of lambs whose Items Diets c d e f diet was supplemented with sunflower oil [10]. Many C A O AO studies have focused on protecting PUFAs from oxidation Ingredients, % as DM basis through the use of antioxidants, and several synthetic Peanut vine 50.0 50.0 50.0 50.0 antioxidants, such as butylated hydroxy anisole (BHA), Corn 23.7 23.7 0.0 0.0 butylated hydroxy toluene (BHT) and alpha tocopherol Wheat bran 2.8 2.8 28.4 28.4 have been successfully employed to prevent or restrict Rapeseed cake 8.3 8.3 3.4 3.4 lipid oxidation in meat products [11]. Fat tissues are the source of many valuable products in Tofu dreg 13.1 13.1 13.1 13.1 the food industry. For example, sheep store excess fat in Soybean oil 0.0 0.0 3.0 3.0 their tails during times of abundant food, and this tail fat Antioxidant 0.0 0.025 0.0 0.025 is used to produce ghee, a type of clarified butter [12]. Salt 0.8 0.8 0.8 0.8 Perirenal fat along with the triceps brachii muscles can CaHPO 0.5 0.5 0.5 0.5 be used to produce hamburger meat [13]. Given that the NaHCO 0.3 0.3 0.3 0.3 generation of flavor volatiles is highly dependent on the 3 cooking method, most studies have focused on the flavor Premix 0.5 0.5 0.5 0.5 development of cooked meat, but there is scant informa- Chemical composition tion about raw meat. The fatty acids and volatiles in raw DM, % 79.8 79.8 80.4 80.4 animal tissues could be considered as the basal compo- DE, MJ/kg 12.9 12.9 13.0 13.0 nents that play a part in the complex reactions between CP, % of DM 15.4 15.4 15.3 15.3 fatty acids and other non-volatiles during cooking; it is Ca, % of DM 1.6 1.6 1.5 1.5 therefore desirable to identify the fatty acids and vola- tiles in fat tissue, as the solvents of volatiles. Because the P, % of DM 0.4 0.4 0.5 0.5 effect of dietary soybean oil supplementation on the Diet was formulated to meet the Feeding Standards of Meat-producing Sheep and Goats (Ministry of Agriculture of P.R. China, 2004) volatiles profile in the raw tissue of lambs is limited, we Diets included four treatments (C, A, O and OA) and are the same as in hypothesized that dietary soybean oil supplementation Tables 2, 3, 4, 5, 6 and Fig. 1 C is the control group; the diet did not contain antioxidants or soybean oil (3 % DM) might increase the level of PUFAs in tail sub- A is the antioxidant group; the diet consisted of the control diet plus cutaneous and perirenal fat tissues of fattening lambs, antioxidant (0.025 % of DM) with coinciding antioxidant supplementation to minimize O is the soybean oil group; the diet consisted of the control diet plus soybean oil (3 % of DM), and the dietary energy and protein levels were PUFA oxidation in fat tissues. adjusted to match those of the control diet Huzhou sheep, renowned for their rapid growth rates OA is the soybean oil plus antioxidant group; the diet consisted of the soybean oil diet plus antioxidant (0.025 % of DM) and high fertility, are among the most common breed of Formulated to provide (per kilogram of DM) 1 200 000 IU of vitamin A, 280 sheep raised in China. Here, we examined the effects of 000 IU of vitamin D, 5 000 mg of vitamin E, 14 000 mg of Zn, 3 500 mg of Mn, dietary supplementation with a UFA (soybean oil) and 3 000 mg of Cu, 200 mg of I, 60 mg of Co and 100 mg of Se antioxidants on the fatty acid and volatiles profile of the tail SF and PF of fattening Huzhou lambs. Plus, a proprietary blend of antioxidants that includes ethoxyquin and silicon dioxide; Novus International Inc., Methods St. Charles, MO, USA), designated as the Antioxidant Animals and management group (A); 3) basal diet supplemented with soybean oil The experimental procedures used here, including the (3 % DM), designated as the Oil group (O); and 4) basal feeding, transport and slaughter of the subject sheep, diet supplemented with both soybean oil and antioxidants, were approved by the Zhejiang University Experimental designated as the Oil and Antioxidant group (OA). All Animal Welfare Ethics Committee. groups were fed equal portions twice daily at 0830 and Thirty-six 7-month-old male Huzhou male lambs 1630 h, and the lambs were given free access to drinking (29.9 kg ± 2.2 kg [mean ± SD]) were randomly divided into water. Feeding trials were conducted for a period of four groups based on a randomized block design, with 7 wks, consisting of 1 wk for adaptation followed by 6 wks each group composed of three units of three lambs. Four of treatment. Feed intake and residual food amounts were dietary treatments (concentrate:forage ratio of 5:5) catego- recorded throughout the testing period. rized by soybean oil and antioxidant as the main effects (Tables 1 and 2) were used, with treatments consisting of Sample collection 1) basal diet without supplementation (C); 2) basal diet At the end of the experiment, all lambs were weighed supplemented with antioxidants (0.025 % DM of Agrado prior to the morning feeding for two consecutive days Peng et al. Journal of Animal Science and Biotechnology (2016) 7:24 Page 3 of 9 Table 2 Fatty acid composition of the diet (percentage of total 1 mL of the upper layer was transferred to a new tube fatty acids) and dried by nitrogen. The FAMEs were dissolved in Fatty acids, % C/A O/OA 0.9 mL of hexane and 0.1 mL of methyl heneicosanoate (1 mg/mL) and then transferred to clean vials prior to C10:0 0.04 0.01 GC analysis. C12:0 0.34 0.19 A GC 6890 N with an FID detector (Agilent Technolo- C14:0 0.32 0.20 gies Inc., CA, USA) equipped with a DB-23 column (30 m C15:0 0.03 0.02 long, 0.25 mm ID, 0.25-μm film) (Agilent Technologies C16:0 8.26 7.93 Inc., CA, USA) was used to analyze the fatty acid profiles C16:1 0.17 0.11 of the samples at injector and detector temperatures of 220 °C and 260 °C, respectively. The temperature program C17:0 0.12 0.10 consisted of an initial temperature of 70 °C, an increase at C18:0 3.39 3.15 a rate of 58 °C/min to 240 °C and a final temperature of C18:1 n9c 14.26 11.38 240 °C for 5 min. Fatty acids were identified by compari- C18:2 n6t 0.20 0.35 son to known external standard mixes of 37 FAMEs C18:2 n6c 17.64 22.23 (Sigma Aldrich, China). Methyl-heneicosanoate was se- C18:3 n3 2.48 2.81 lected as the internal standard, with the quantity of each fatty acid calculated according to the relative peak area of C20:1 0.72 0.31 the internal standard. C20:5 n3 0.13 0.07 C22:1 n9 1.68 0.86 Volatile compounds analysis C23:0 0.06 0.12 Headspace solid phase micro-extraction (SPME) coupled C24:0 0.04 0.06 with gas chromatography-mass spectrometry (GC-MS) was C22:6 n3 0.02 0.01 used to analyze the volatiles content of fat tissue, as de- scribed elsewhere [15]. Briefly, SPME with 50/30 mm divi- C24:1 n9t 0.10 0.10 nylbenzene/carboxen/polydimethylsiloxane fiber was used Saturated 12.60 11.77 to extract the volatiles from 1-g samples of fat tissues at Unsaturated 37.40 38.23 120 °C. A DB-5 capillary column (30 m × 0.25 mm × 0.25 mm) (Agilent Technologies Inc., CA, USA) was used and transported to a slaughterhouse after being fasted to analyze the volatiles. After desorption of SPME at 250 °C for 24 h. The total PF and right side of the tail fat were for 5 min, volatiles were separated under the following sliced following removal of the vessels and connective chromatographic conditions: GC oven temperatures were tissues, and approximately 20 g of the PF and tail SF increased from 40 to 250 °C at a rate of 38 °C/min and then were subsampled and vacuum-packed after slaughter. held at 250 °C for 5 min, with helium used as the carrier The samples were stored at 4 °C for 24 h, followed by gas at a flow rate of 0.8 mL/min. The electron impact en- storage at −80 °C for the subsequent determination of ergy was set at 70 eV, and data were collected in the range volatiles and fatty acids. of m/z 40–650. The Wiley library and mass spectral data- base (NIST 2002, Washington, DC, USA) coupled to the Fatty acids analysis Kovats retention indices taken from a series of standards Fatty acid methyl esters (FAMEs) were produced from (C6-C25 n-alkanes) were used to identify the mass spectra 20 mg of fat samples via the one-step trans-esterification of the volatile compounds. method, in accordance with the procedures described by Rule [14]. The FAMEs were dissolved in 0.9 mL of hex- Statistical analysis ane and 0.1 mL of methyl heneicosanoate as an internal Growth performance, fatty acid content and volatiles pro- standard (1 mg/mL) and then transferred to clean vials file data were analyzed using the GLM procedure of the for gas chromatography (GC) analysis according to the SAS software system (version 9.1). The model included procedures described in a previous study [15]. In brief, soybean oil, antioxidants and the interaction between soy- 20-mg fat samples were placed in 10-mL screw-capped bean oil and antioxidants. The means were compared tubes, to which 1 mL each of a boron trifluoride metha- when the interaction terms of the model were significant nol solution and methanol were added. The tubes were (P < 0.05) using the LAMEANS and PDIFF separation of then placed in an 80 °C water bath for 2 h and vortexed the entire group. Discriminant function analysis (DFA) every 5 min. After the tubes had cooled, 1.5 mL of hex- was performed to distinguish the characteristics of the ane and 1.5 mL of double distilled water were added and volatiles among the four groups. All data were normalized thoroughly mixed. Upon cooling to room temperature, with a log10 transformation prior to DFA. Peng et al. Journal of Animal Science and Biotechnology (2016) 7:24 Page 4 of 9 Results As shown in Table 5, dietary soybean oil supplemen- Growth performance tation increased the content of total acids (P = 0.03) As shown in Table 3, no significant effect of soybean oil and decreased the contents of methyl 2,8-dimethylde- and antioxidant on growth performance was detected, but canoate, 2-hexyl-1-decanol and 2-pentadecanone in SF final body weight (P = 0.13) and average daily gain (ADG) (P < 0.05); moreover, soybean oil supplementation led (P = 0.08) were slightly reduced in sheep undergoing the to slightly decreased E-2-nonenal (P = 0.11) levels, and soybean oil treatment. Antioxidant supplementation tended increased ethyl caprinate, decanoic acid and undecanoic to decrease dry matter intake (DMI) (P = 0.10), final body acid (0.05 < P < 0.20) levels. No volatile compounds were weight (P = 0.07) and the ADG of lambs (P =0.07). affected by antioxidant treatment or by the interaction between soybean oil and antioxidant. As shown in Table 6, levels of E-2-octenal, E,E-2,4- Fatty acid profile decadienal, 2-undecenal and ethyl 9-decenoate tended to The primary effects of soybean oil and antioxidant sup- decrease in response to soybean oil supplementation plementation on the fatty acid profiles of SF and PF are (0.05 < P < 0.20), but no volatile compounds were af- shown in Table 4. Palmitic acid (16:0), oleic acid (18:1) fected by the antioxidant treatment. The total content of and stearic acid (18:0) were the three major fatty acids aldehydes was affected by the interaction between soy- in both SF and PF, accounting for more than 85 % of the bean oil and antioxidant supplementation (P = 0.03). total fatty acid content. All of the volatile compounds detected in SF and PF For SF, soybean oil supplementation only increased the were subjected to discriminant function analysis (DFA) content of C18:2 n6t (P = 0.03), whereas antioxidant sup- (Fig. 1). The DFA plot based on the volatiles profile of plementation increased the contents of C17:0 (P = 0.03), SF is shown in Fig. 1a. In DF1 (74.7 %), the C group was C18:3 n3 (P = 0.02) and C18:2 n6c (P = 0.06). No fatty distinguished from the other three groups (A, O and OA acid was affected by the interaction of soybean oil and groups), but those groups were not separated from one antioxidant. another; however, the O group was separated from the For PF, soybean oil supplementation increased the OA group in DF2 (16.1 %). The DFA plot based on the content of C18:0 (P < 0.01) and decreased the propor- volatiles profile of PF is shown in Fig. 1b. In DF1 tion of total UFA (P = 0.03), which was mainly attrib- (66.7 %), the C and CA groups were separated from the uted to decreases in C18:1 (P = 0.01) and C22:1 n9 O and OA groups, but the C group was not distin- contents (P < 0.01). Antioxidant supplementation did guished from the CA group, and the O group was not not affect the fatty acid composition of PF (P > 0.05). separated from the OA group. In DF2 (19.7 %), the C The interaction between soybean oil and antioxidant group was separated from the CA group, and the O significantly affected the total amount of FA (P = 0.03) group was separated from the OA group. and the C22:1n9 content of the PF (P = 0.03). Discussion Volatile compounds profile Growth performance A total of 35 volatile compounds were identified in SF To maintain equal energy and protein levels between the and PF and classified according to their chemical nature control and soybean oil-supplemented diets, a higher as acids, aldehydes, alcohols, esters and others (Tables 5 percentage of wheat bran was used instead of corn in and 6). Aldehydes and esters were the two major types the soybean oil diet, which might increase the satiety of of volatile compounds in both fat tissues, accounting for lambs in groups O and OA and thus reduce their DMI approximately 70 % of the total volatiles detected. and final body weights. Moreover, the effects of dietary Table 3 Effects of supplementation with soybean oil, antioxidant or soybean oil plus antioxidant on growth of fattening lambs Items Diet SEM P-value a b c CA O AO O A O× A Number of lambs 9999 Initial body weight, kg 29.8 30.0 30.0 29.7 0.58 Final body weight, kg 37.5 35.6 35.8 35.1 0.61 0.13 0.07 0.39 Dry matter intake, g/d 1213 1137 1160 1078 42.0 0.22 0.10 0.95 Average daily gain, g/d 188 147 148 141 11.3 0.08 0.07 0.16 The effect of soybean oil, the same as in Tables 4, 5 and 6 The effect of antioxidant, the same as in Tables 4, 5 and 6 The interactive effect of soybean oil and antioxidant, the same as in Tables 4, 5 and 6 Peng et al. Journal of Animal Science and Biotechnology (2016) 7:24 Page 5 of 9 Table 4 Effects of supplementation with soybean oil, antioxidant performance of finishing lambs [16, 17]; on the contrary, or soybean oil plus antioxidant on fatty acid composition of several studies have reported significantly negative effects subcutaneous and perirenal fat tissue in fattening lambs of dietary soybean oil on the growth performances of both Fatty acids, Diet RMSE P-value steers and lambs and suggested that the UFA in the soy- g/100 g FAME CA O AO O A O×A bean oil may impair rumen fermentation and fiber digest- ibility [18, 19]. Potential negative effects of UFAs on Subcutaneous fat tissue b rumen fermentation should therefore be of concern. Total FA 209 211 213 199 44.92 0.79 0.73 0.60 Contrary to what we expected, dietary antioxidant sup- C10:0 0.34 0.34 0.31 0.36 0.15 0.94 0.65 0.64 plementation tended to negatively affect lamb growth. C12:0 0.39 0.32 0.42 0.37 0.15 0.47 0.26 0.88 Agrado Plus is a commercial antioxidant used in feed, and C14:0 4.64 4.15 4.81 4.47 0.88 0.41 0.18 0.81 the results of several studies – including our own previous C14:1 0.81 0.93 0.75 0.95 0.60 0.92 0.44 0.86 research – have demonstrated its beneficial effect on the health and performance of dairy cattle [20, 21]. Here, the C15:0 1.08 1.22 1.08 1.19 0.29 0.87 0.21 0.88 reasons for the negative effects of antioxidant supplemen- C16:0 25.3 24.0 25.8 25.1 2.13 0.29 0.18 0.71 tation on lamb growth were undetermined; it may simply C16:1 2.98 2.60 2.93 2.81 0.97 0.81 0.47 0.69 be due to differences in the physiologies of sheep and C17:0 1.58 1.86 1.46 1.65 0.31 0.13 0.03 0.66 dairy cattle. C18:0 14.8 14.8 13.8 13.3 4.15 0.40 0.86 0.85 C18:1 43.0 44.0 43.2 44.0 2.82 0.90 0.36 0.97 Fatty acid profile Similar to the increased C18:2 in tail SF observed here, diet- C18:2 n6t 0.89 1.00 1.13 1.04 0.18 0.03 0.93 0.11 ary PUFA-rich soybean oil supplementation improved the C18:2 n6c 3.74 4.20 3.75 4.17 0.65 0.97 0.06 0.93 content of C18:2 in the intramuscular fat of goats and C18:3 n6 0.11 0.11 0.13 0.08 0.07 0.94 0.37 0.35 lambs [4, 19]. Because C18:2 is the main fatty acid in soy- C18:3 n3 0.41 0.51 0.40 0.51 0.12 0.90 0.02 0.95 bean oil, the increased proportion of C18:2 in the SF may UFA 66.7 68.1 66.1 66.9 3.05 0.40 0.31 0.76 be due to the dietary C18:2 that was not subjected to U/S 2.03 2.16 1.96 2.05 0.26 0.33 0.24 0.84 biohydrogenation in the rumen. In our previous study of dairy cattle, dietary antioxidants counteracted the negative Perirenal fat tissue b effects of dietary low saturated fats (mainly C18:1) and in- Total FA 145 114 105 119 28.47 0.09 0.41 0.03 creased C18:1 levels in the milk [21], which suggested that C10:0 0.23 0.21 0.20 0.17 0.07 0.16 0.31 0.97 antioxidant supplementation had a positive influence on C12:0 0.31 0.33 0.33 0.42 0.29 0.59 0.62 0.72 UFA accumulation. In this study, however, antioxidant C14:0 3.32 3.11 2.99 2.68 0.64 0.10 0.25 0.82 supplementation increased the concentrations of both C15:0 0.84 0.84 0.86 0.84 0.11 0.89 0.90 0.75 C18:2 and C18:3 in SF regardless of whether it was ingested as part of a normal diet or a diet enriched with C16:0 24.5 23.0 23.9 22.4 2.49 0.53 0.11 1.00 soybean oil, providing a positive signal that the use of anti- C17:0 1.64 1.78 1.51 1.55 0.13 0.00 0.07 0.28 oxidants might improve the nutritional value of Huzhou C18:0 36.2 37.3 39.2 43.3 4.14 0.00 0.09 0.30 lamb tail SF. C18:1 27.4 27.9 25.8 23.6 3.06 0.01 0.42 0.21 Differences between internal (perirenal) and external C18:2 n6c 3.70 3.92 3.82 3.55 1.05 0.73 0.95 0.50 (subcutaneous) fat deposits have been widely demonstrated. C18:3 n6 0.18 0.17 0.18 0.17 0.05 0.88 0.50 0.88 In this study, more UFAs were detected in SF, whereas more SFAs were detected in PF, accounting for 70 % of the C18:3 n3 0.53 0.45 0.48 0.44 0.19 0.62 0.34 0.74 total fatty acids in PF. This finding is consistent with the C20:0 0.52 0.53 0.49 0.58 0.14 0.88 0.28 0.44 higher SFA concentrations previously observed in internal C20:1 0.36 0.28 0.23 0.22 0.15 0.10 0.43 0.52 (kidney) fat compared with external fat depots [22]. As Lee C22:1 n9 0.28 0.21 0.07 0.14 0.09 0.00 0.96 0.03 et al. [23] reported, stearoyl-CoA desaturase (SCD) activity UFA 32.5 32.9 30.6 28.1 4.22 0.03 0.49 0.32 was higher in SF than in PF, which partially explains the U/S 0.48 0.50 0.44 0.40 0.09 0.02 0.57 0.31 higher SFA proportion observed in the PF in this study. RMSE root mean square error, the same as in Tables 5 and 6 The fatty acid profile in PF changed in a different manner The amount of total FA is expressed as mg/g fat tissue than did that of SF in response to dietary supplementation regardless of whether the supplement was soybean oil or soybean oil supplementation on ruminant growth per- antioxidant, similar to observations made by Lee et al. formance were not consistent. Based on our findings [24], who supplemented the diet of lambs with ground both here and in a previous study of Huzhou lambs, soy- whole-fat soybeans. Moreover, Berthelot et al. showed bean oil supplementation did not influence the growth that the differential uptake of FA from the rumen Peng et al. Journal of Animal Science and Biotechnology (2016) 7:24 Page 6 of 9 Table 5 Effects of supplementation with soybean oil, antioxidant or soybean oil plus antioxidant on volatile profiles in subcutaneous fat tissues of fattening lambs a b c Component Abb. RI CSID Diet RMSE P-value C A O AO O A O*A Aldehydes 36.5 36.4 35.0 32.6 14.50 0.61 0.81 0.82 Hexanal Ad1 798 5949 - 0.7 1.9 - - - - E-2-Heptenal Ad2 955 4446437 1.3 1.2 1.1 0.8 1.06 0.41 0.62 0.82 Phenylacetaldehyde Ad3 1040 13876539 2.1 2.1 2.0 1.6 1.35 0.49 0.68 0.64 E-2-Octenal Ad4 1056 4446445 1.6 2.0 1.4 3.4 2.99 0.57 0.29 0.47 Nonanal Ad5 1104 29029 12.1 13.5 14.3 7.2 8.07 0.48 0.33 0.14 E-2-Nonenal Ad6 1157 4446456 12.3 11.1 8.0 8.6 6.45 0.15 0.92 0.70 E,E-2,4-Decadienal Ad7 1295 4446470 4.1 3.4 4.0 4.1 2.26 0.67 0.72 0.60 2-Undecenal Ad8 1368 4446477 3.0 2.5 2.3 7.0 6.46 0.42 0.38 0.27 Esters 34.4 39.1 39.8 42.5 14.36 0.40 0.48 0.84 Ethyl octanoate Es1 1193 7511 1.8 1.1 1.0 4.7 4.35 0.36 0.34 0.16 Methyl decanoate Es2 1328 7759 3.0 1.1 1.3 5.0 5.70 0.59 0.67 0.17 Ethyl cyclohexanepropanoate Es3 1345 55387 5.1 9.8 6.5 5.0 7.00 0.50 0.54 0.22 Methyl 2,8-dimethyldecanoate Es4 1353 487217 3.0 2.9 1.1 1.1 2.17 0.02 0.90 0.96 Ethyl 9-decenoate Es5 1389 455568 3.2 2.0 2.8 1.8 1.91 0.64 0.12 0.89 Ethyl caprinate Es6 1398 7757 2.1 5.0 12.0 7.4 10.33 0.11 0.83 0.31 Methyl 2,4,6-trimethylundecanoate Es7 1487 487035 0.3 0.3 0.5 0.5 0.34 0.14 0.78 0.85 Methyl undecanoate Es8 1490 14847 2.0 2.6 1.5 1.9 1.57 0.28 0.42 0.85 Ethyl 9-oxononanoate Es9 1537 17861 - 3.6 - - - - - Methyl laurate Es10 1554 7847 0.8 0.7 0.7 0.8 0.48 0.81 0.78 0.58 Ethyl laurate Es11 1597 7512 3.3 1.2 1.9 2.4 2.87 0.92 0.43 0.20 Geranyl isovalerate Es12 1606 4515295 0.8 1.3 0.7 0.8 0.79 0.27 0.23 0.51 Methyl 2,6-dimethyltridecanoate Es13 1651 487205 1.1 2.1 2.0 1.6 1.70 0.70 0.67 0.28 Methyl myristate Es14 1769 29024 2.2 1.8 3.5 2.4 2.97 0.38 0.45 0.73 Ethyl myristate Es15 1793 29023 5.6 3.6 4.3 7.1 7.68 0.69 0.89 0.39 Acids 8.1 10.7 12.4 14.7 5.11 0.03 0.20 0.92 (2E)-2-Methyl-2-nonenoic acid Ac1 1269 4724999 1.7 1.4 2.8 2.1 2.20 0.28 0.52 0.79 Decanoic acid Ac2 1355 2863 2.2 3.0 4.5 6.1 4.00 0.07 0.42 0.76 Undecanoic acid Ac3 1465 7888 0.5 0.7 0.8 0.9 0.48 0.15 0.23 0.74 Lauric acid Ac4 1537 3756 - 1.5 1.4 1.7 - - - Tridecylic acid Ac5 1621 12013 0.7 2.0 1.2 0.9 1.49 0.57 0.33 0.17 Alcohols 12.8 9.0 8.9 8.1 6.22 0.29 0.30 0.50 Heptan-1-ol Al1 969 7837 4.0 3.0 3.8 2.7 3.91 0.86 0.47 0.94 1-Octanol Al2 1069 932 1.1 1.1 1.1 1.1 0.96 0.91 0.99 0.89 2-Methyl-1-dodecanol Al3 1492 38544 4.4 2.0 2.2 2.8 3.87 0.62 0.50 0.28 2-Hexyl-1-decanol Al4 1790 86034 3.4 2.9 1.8 1.5 1.78 0.03 0.55 0.96 Others 8.2 4.8 3.8 2.2 3.50 0.01 0.06 0.46 Toluene Ot1 762 1108 3.7 0.9 1.4 - - - - 2-Pentadecanone Ot2 1696 55242 4.7 3.8 2.4 2.1 2.42 0.03 0.48 0.71 All volatile compounds were grouped according to chemical categories. Ad, Ac, Al, Es and Ot are abbreviations for the aldehyde, acid, alcohol, ester and “other” groups, respectively, the same as in Table 6 RI, retention indices of individual compounds relative to C6-C25 n-alkanes, the same as in Table 6 CSID, ChemSpider ID of each chemical (http://www.chemspider.com/), the same as in Table 6 Peng et al. Journal of Animal Science and Biotechnology (2016) 7:24 Page 7 of 9 Table 6 Effects of supplementation with soybean oil, antioxidant or soybean oil plus antioxidant on volatile profiles in perirenal fat tissues of fattening lambs Component Abb. RI CSID Diet RMSE P-value C A O AO O A O*A Aldehydes 34.3 41.4 38.6 31.7 8.65 0.37 0.98 0.03 Hexanal Ad1 798 5949 1.6 - 4.2 2.6 E-2-Heptenal Ad2 955 4446437 2.0 2.2 2.4 1.6 2.02 0.90 0.68 0.53 Phenylacetaldehyde Ad3 1040 13876539 1.6 1.6 6.6 0.3 5.08 0.31 0.09 0.08 E-2-Octenal Ad4 1056 4446445 1.5 1.9 0.5 0.7 1.52 0.08 0.61 0.83 Nonanal Ad5 1104 29029 3.6 4.5 4.8 4.9 2.79 0.45 0.66 0.68 E-2-Nonenal Ad6 1157 4446456 2.1 4.3 2.4 1.9 2.85 0.31 0.42 0.19 E,E-2,4-Decadienal Ad7 1295 4446470 19.5 24.7 16.3 18.1 8.98 0.10 0.29 0.59 2-Undecenal Ad8 1368 4446477 3.0 3.6 1.4 2.3 2.72 0.14 0.46 0.86 Esters 34.8 33.9 34.9 41.9 8.14 0.17 0.31 0.17 Ethyl octanoate Es1 1193 7511 3.6 3.0 4.6 4.2 3.05 0.34 0.68 0.89 Methyl decanoate Es2 1328 7759 10.5 6.1 7.6 10.5 5.74 0.73 0.75 0.10 Ethyl cyclohexanepropanoate Es3 1345 55387 1.8 2.1 1.8 1.5 1.47 0.61 0.92 0.55 Methyl 2,8-dimethyldecanoate Es4 1353 487217 1.5 2.5 1.4 2.3 2.56 0.87 0.32 0.95 Ethyl 9-decenoate Es5 1389 455568 2.1 2.3 1.8 1.2 1.13 0.10 0.63 0.26 Ethyl caprinate Es6 1398 7757 3.4 5.1 2.8 5.4 5.95 0.95 0.31 0.83 Methyl 2,4,6-trimethylundecanoate Es7 1487 487035 0.3 0.6 0.7 1.8 1.10 0.06 0.13 0.33 Methyl undecanoate Es8 1490 14847 2.5 2.7 2.5 3.4 2.68 0.73 0.60 0.72 Ethyl 9-oxononanoate Es9 1537 17861 2.3 - 3.1 6.6 Methyl laurate Es10 1554 7847 0.8 1.0 3.4 1.5 2.21 0.13 0.37 0.27 Ethyl laurate Es11 1597 7512 1.6 2.5 1.1 2.2 1.77 0.56 0.16 0.81 Geranyl isovalerate Es12 1606 4515295 0.7 1.4 0.8 0.8 0.81 0.32 0.23 0.23 Methyl 2,6-dimethyltridecanoate Es13 1651 487205 0.6 0.8 2.2 0.6 1.30 0.20 0.22 0.08 Methyl myristate Es14 1769 29024 1.4 3.0 0.9 1.9 3.10 0.44 0.25 0.76 Ethyl myristate Es15 1793 29023 1.8 3.5 3.0 2.5 3.88 0.94 0.70 0.42 Acids 16.0 12.0 11.1 14.3 11.15 0.74 0.92 0.36 (2E)-2-Methyl-2-nonenoic acid Ac1 1269 4724999 4.1 4.8 3.8 3.5 2.14 0.34 0.81 0.52 Decanoic acid Ac2 1355 2863 - - 1.8 1.5 Undecanoic acid Ac3 1465 7888 9.6 1.9 1.1 3.1 11.71 0.40 0.51 0.25 Tridecylic acid Ac5 1621 12013 3.1 1.7 3.1 1.9 1.94 0.85 0.08 0.93 (7Z)-7-Tetradecenoic acid Ac7 1777 4471826 0.7 1.5 0.9 0.9 0.67 0.41 0.13 0.08 Alcohols 7.9 8.7 10.1 6.8 3.69 0.92 0.35 0.11 Heptan-1-ol Al1 969 7837 1.5 1.2 2.1 0.8 1.12 0.80 0.06 0.26 1-Octanol Al2 1069 932 3.3 3.1 3.0 2.1 1.82 0.40 0.45 0.63 2-Methyl-1-dodecanol Al3 1492 38544 1.8 2.9 3.3 3.4 2.85 0.34 0.54 0.61 2-Hexyl-1-decanol Al4 1790 86034 1.5 2.1 2.5 1.3 2.25 0.96 0.72 0.24 Others 7.0 4.0 5.3 5.5 3.26 0.92 0.23 0.18 Toluene Ot1 762 1108 0.8 1.1 - 1.2 2-Pentadecanone Ot2 1696 55242 6.2 3.3 5.3 4.3 3.37 0.95 0.12 0.42 contributes to variations in trans-fatty acid proportions Volatile compounds profile in the PF, SF and muscles in response to vitamin E Volatile components are not necessarily odor-active. As supplementation [25]. reviewed by Watkins et al., only 15 of 187 volatiles were Peng et al. Journal of Animal Science and Biotechnology (2016) 7:24 Page 8 of 9 Fig. 1 DFA plots of volatile profiles of subcutaneous (a) and perirenal (b) fat tissues from lambs fed normal diets (■, C), diets supplemented with soybean oil (▲, O), diets supplemented with antioxidant (●, A) and diets supplemented with soybean oil plus antioxidant (▼, AO) identified as the primary components of lamb aroma based but its concentration decreased in response to dietary on a gas chromatography − olfactometry (GC-O) analysis, soybean oil supplementation, suggesting that the intensity including the aldehydes E,E-2,4-decadienal, Z-2-nonenal, of “fatty” or “fried”-like flavors of PF was more subdued. E-2-heptenal, methional, E-2-nonenal, decanal, 2,4-E,E- Compared with the effects of soybean oil supplementa- heptadienal, octanal and E-2-octenal [10]. Meanwhile, one tion, antioxidant supplementation triggered fewer changes indicator, termed the odor-activity value, was calculated in both SF and PF. In SF, although antioxidant supplemen- and used to represent the contribution of volatiles to food tation led to higher concentrations of C18:2 and C18:3, flavor [26]. Bueno et al. built a partial least-squares model the fact that we did not detect a simultaneous increase in based on the odor-activity value of 32 volatiles and con- the oxidative by-products (aldehydes) of these UFAs is an cluded that alkenals and alkadienals have negative effects indication that antioxidant supplementation may improve on the intensity of lamb flavor and that E,E-2,4-decadienal anti-oxidative performance and thus hinder the progress and E-2-nonenal were the most abundant volatiles [27]. of UFA oxidation. In the PF, the interaction effect between We found similar patterns in this study: the main alde- soybean oil and antioxidant supplementation on aldehydes hydes in SF (such as nonanal, E-2-nonenal and E,E-2,4- suggested that the presence of the antioxidant slows the decadienal) and those in PF (E,E-2,4-decadienal) largely rate of accumulation of oxidative by-products. Thus, determine the flavor characteristics of SF and PF. although the antioxidant did not induce any direct flavor- When soybean oil was added to the lambs’ diet, the related changes in the composition of the volatiles, it may slight decrease in E-2-nonenal (P = 0.15) observed in the suppress UFA oxidation in fat tissues and thus have an SF was inconsistent with the increase in C18:2, as E-2- indirect positive effect on meat flavor. nonenal is the oxidative product of C18:2, suggesting that To visually represent the different responses of SF and the extent of oxidation in SF might be lower than what we PF to dietary soybean oil and antioxidant supplementa- assumed, but the exact reasons for this phenomenon tion, given the complexity of the factors that determine remain unknown. Moreover, the addition of soybean oil the flavor of fat, the DFA plots of the volatile contents tended to increase the content of the volatile decanoic provide an intuitive outline of the differences between acid (P = 0.07). The odor of decanoic acid is reported to each sample. From Fig. 1a, it can be seen that soybean be positively associated with the oxidation of wine, con- oil supplementation might change the flavor of SF when tributing to the “animal”, “bitterness” and “dairy” charac- no antioxidants are added (74.7 %, C vs O), but less so teristics of wine [28]. Enhanced decanoic acid content when the antioxidant is added (16.1 %, A vs AO); anti- would therefore suggest an increase in SF bitterness as a oxidant supplementation, meanwhile, induced large dif- result of soybean oil supplementation. ferences in the absence of soybean oil (74.7 %, C vs A) In regard to PF, given that the odor threshold of E-2- but did not trigger obvious changes when delivered in octenal is only “4”– that is, the flavor of E-2-octenal conjunction with soybean oil supplementation (16.1 %, O becomes recognizable at concentrations above 4 ng/g vs OA). Thus, the effect of soybean oil supplementation tissue – and despite the content of E-2-octenal decreasing on SF flavor was dependent on whether or not the antioxi- by 1 and 1.2 % with soybean oil supplementation (C vs O: dant was present. As seen in ure 1b, soybean oil supple- 1.5 % vs 0.5 %; A vs AO: 1.9 % vs 0.7 %), the flavor of the mentation led to clear changes when the antioxidant was PF still became less “green, nutty and fatty”,descriptors added (66.7 %, C/CA vs O/OA) and the antioxidant alone that depict the typical flavor of E-2-octenal. Moreover, also altered the volatiles composition (21.9 %, C vs CA, O E,E-2,4-decadienal (with a typical flavor described as “fatty vs OA), but the extent of change caused by the latter sce- and fried foods”) was the primary aldehyde found in PF, nario was less than that of soybean oil supplementation. Peng et al. Journal of Animal Science and Biotechnology (2016) 7:24 Page 9 of 9 We can therefore infer that dietary soybean oil supple- 6. Elmore JS, Cooper SL, Enser M, Mottram DS, Sinclair LA, Wilkinson RG, et al. Dietary manipulation of fatty acid composition in lamb meat and its effect mentation had an effect on PF flavor independent of the on the volatile aroma compounds of grilled lamb. Meat Sci. 2005;69:233–42. presence or absence of the antioxidant. 7. Sañudo C, Enser ME, Campo MM, Nute GR. Maŕ ıa G, Sierra I et al. Fatty acid composition and sensory characteristics of lamb carcasses from Britain and Spain. Meat Sci. 2000;54:339–46. Conclusions 8. Nute GR, Richardson RI, Wood JD, Hughes SI, Wilkinson RG, Cooper SL, et al. In summary, dietary soybean oil supplementation im- Effect of dietary oil source on the flavour and the colour and lipid stability of lamb meat. Meat Sci. 2007;77:547–55. proved the UFA content in tail SF, and antioxidant supple- 9. Scollan ND, Dannenberger D, Nuernberg K, Richardson I, MacKintosh S, mentation further enhanced UFAs by suppressing the Hocquette J-F, et al. Enhancing the nutritional and health value of beef accumulation of oxidative volatiles, thus interacting with lipids and their relationship with meat quality. Meat Sci. 2014;97:384–94. 10. Watkins PJ, Frank D, Singh TK, Young OA, Warner RD. Sheepmeat Flavor and the effect of soybean oil on SF flavor discrimination. Diet- the Effect of Different Feeding Systems: A Review. J Agric Food Chem. 2013; ary soybean oil supplementation induced an decrease in 61:3561–79. the levels of saturated fatty acids and aldehydes in PF. 11. Chastain MF, Huffman DL, Hsieh WH, Cordray JC. Antioxidants in Restructured Beef/Pork Steaks. J Food Sci. 1982;47:1779–82. Antioxidant supplementation, however, had little effect on 12. Kashan NEJ, Azar GHM, Afzalzadeh A, Salehi A. Growth performance and the fatty acid and volatiles composition in the PF. carcass quality of fattening lambs from fat-tailed and tailed sheep breeds. Small Rumin Res. 2005;60:267–71. 13. Turner TD, Aalhus JL, Mapiye C, Rolland DC, Larsen IL, Basarab JA, et al. Abbreviations Effects of diets supplemented with sunflower or flax seeds on quality and ADG: average daily gain; BHA: butylated hydroxy anisole; BHT: butylated fatty acid profile of hamburgers made with perirenal or subcutaneous fat. hydroxy toluene; CLA: conjugated linoleic acid; DFA: discriminant function Meat Sci. 2015;99:123–31. analysis; DMI: dry matter intake; FAMEs: fatty acid methyl esters; GC: gas 14. Rule DC. Direct transesterification of total fatty acids of adipose tissue, and chromatography; GC-MS: gas chromatography-mass spectrometry; GC-O: gas of freeze-dried muscle and liver with boron-trifluoride in methanol. Meat chromatography − olfactometry; PF: perirenal fat tissue; PUFA: polyunsaturated Sci. 1997;46:23–32. fatty acids; SF: subcutaneous fat tissue; SFA: saturated fatty acids; SPME: solid 15. Peng Y-J, Wang J-K, Ren D-X, Lin J, Liu J-X. Different patterns of volatile phase micro-extraction; UFA: unsaturated fatty acid. compounds and fatty acid profiles in the adipose tissues of male and female Hu sheep. Acta Agric Scand Sect A Anim Sci. 2012;62:153–8. Competing interests 16. Berthelot V, Bas P, Pottier E, Normand J. The effect of maternal linseed The authors declare that they have no competing interests. supplementation and/or lamb linseed supplementation on muscle and subcutaneous adipose tissue fatty acid composition of indoor lambs. Meat Authors’ contributions Sci. 2012;90:548–57. YJP carried out the study design, data interpretation and manuscript writing 17. Mao H-L, Wang J-K, Zhou Y-Y, Liu J-X. Effects of addition of tea saponins and editing; JKW was involved in the study design, data interpretation and and soybean oil on methane production, fermentation and microbial manuscript editing; JL was involved in the animal experiment; JXL was involved population in the rumen of growing lambs. Livest Sci. 2010;129:56–62. in the study design, data interpretation and manuscript editing. All authors read 18. Engle TE, Spears JW, Fellner V, Odle J. Effects of soybean oil and dietary and approved the final manuscript. copper on ruminal and tissue lipid metabolism in finishing steers. J Anim Sci. 2000;78:2713–21. 19. Bhatt RS, Soren NM, Tripathi MK, Karim SA. Effects of different levels of coconut Acknowledgments oil supplementation on performance, digestibility, rumen fermentation and This study was financed by the Innovation Team Program of Zhejiang province carcass traits of Malpura lambs. Anim Feed Sci Technol. 2011;164:29–37. (2011R50025). We thank the staff at Changda Sheep Farm for their assistance in 20. He M, Armentano LE. Effect of fatty acid profile in vegetable oils and animal feeding and care. antioxidant supplementation on dairy cattle performance and milk fat depression. J Dairy Sci. 2011;94:2481–91. Author details 21. Wang YM, Wang JH, Wang C, Chen B, Liu JX, Cao H, et al. Effect of different Laboratory of Ruminant Nutrition, College of Animal Sciences, Zhejiang rumen-inert fatty acids supplemented with a dietary antioxidant on performance University, 866 Yuhangtang Road, Hangzhou, 310058 Zhejiang, P. R. China. and antioxidative status of early-lactation cows. J Dairy Sci. 2010;93:3738–45. College of Biological, Chemical Science and Engineering, Jiaxing University, 22. Horcada-Ibáñez A, Beriain-Apesteguía MJ, Lizaso-Tirapu G, Insausti-Barrenetxea 118 Jiahang Road, 314001 Jiaxing, Zhejiang, P. R. China. K, Purroy-Unanua A. Effect of sex and fat depot location on fat composition of Rasa Aragonesa lambs. Agrociencia. 2009;43:803–13. Received: 20 July 2015 Accepted: 28 March 2016 23. Lee J-H, Yamamoto I, Jeong J-S, Nade T, Arai T, Kimura N. Relationship between adipose maturity and fatty acid composition in various adipose tissues of Japanese Black, Holstein and Crossbred (F1) steers. 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Journal of Animal Science and BiotechnologySpringer Journals

Published: Apr 12, 2016

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