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METABOLISM AND NUTRITION |
-Tocopherol Content of Whole Body, Liver, and Plasma of Chickens Without Variations in Intestinal Apparent AbsorptionGrup de Recerca en Nutrició, Maneig i Benestar Animal, Departament de Ciència Animal i dels Aliments, Facultat de Veterinària, Universitat Autònoma de Barcelona, 08193, Bellaterra, Barcelona, Spain
1 Corresponding author: egmanzanilla{at}gmail.com
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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-tocopherol apparent absorption and deposition in broiler chickens at 2 ages (20 and 39 d). The dietary fat was a mixture of linseed and fish oil, rich in polyunsaturated fatty acids (PUFA). The experimental treatments were the result of 4 levels of supplementation with -tocopheryl acetate (0, 100, 200, and 400 mg/kg; E0, E100, E200, and E400 treatments, respectively) and 4 dietary oil inclusion levels (2, 4, 6, and 8%; O2, O4, O6, and O8 treatments respectively). Almond husk was used as an energy dilutor in the high-fat diets. Apparent absorption of total fatty acids was high in all treatments averaging 88% and was higher with high fat dietary inclusion level. -Tocopheryl acetate hydrolysis and apparent absorption of -tocopherol were similar in both ages and were not affected by fat inclusion level, except for a reduction of the absorption in the low-fat diet (O2) in the E100 treatment at 20 d of age. Despite this lack of differences in hydrolysis and absorption, higher-fat PUFA diets induced lower concentrations of free -tocopherol in the excreta, at high -tocopherol doses, suggesting an increase in the destruction of -tocopherol by lipid oxidation in the gastrointestinal tract. Similarly, total and hepatic -tocopherol deposition was lower in the birds fed high-PUFA diets in the E200- and E400-supplemented birds, possibly due to a destruction of vitamin E when protecting these PUFA from lipid peroxidation. -Tocopherol concentration in liver and, to a lesser extent, in plasma was a useful indicator of the degree of response of this vitamin to different factors that can affect its bioavailability; however, in the present experiment, CV were too high to use liver and plasma concentrations as estimators of total body vitamin E.
Key Words: chicken • fat • unsaturated • vitamin E
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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-tocopherol. It is common to include vitamin E in poultry feeds in the form of -tocopheryl acetate (-TA). The ester bond protects vitamin E from oxidation during processing and storage of food. Once in the intestine, the ester is hydrolyzed, and -tocopherol becomes active. In spite of the importance of vitamin E, data regarding its intestinal uptake in chickens is scarce and highly variable (Sklan et al., 1982; Engberg et al., 1996; Knarreborg et al., 2004). It is known that -tocopherol can be absorbed only in its free form (Cohn et al., 1992), and it is accepted that its intestinal uptake occurs following the processes necessary for digestion and absorption of dietary fats (Cohn et al., 1992; Surai, 1999). Unlike vitamin A, -tocopherol is not reesterified following absorption, and, therefore, body tissues would contain -tocopherol, not esters. All tissues in general respond to vitamin E supplementation, but the turnover rates differ greatly among them. Lung, liver, and small intestine have the greatest turnover rates, and muscle, brain, and spinal chord have the lowest (Ingold et al., 1987). Supplementation with this vitamin above NRC (1994) requirements has been shown to increase shelf life of poultry meat (Grau et al., 2001) and vitamin E concentration in poultry tissues (Sheehy et al., 1991). The source and dosage of the vitamin supplement can affect vitamin E intestinal uptake and, therefore, its bioavailability (Jensen et al., 1999), but other dietary factors may be important (Villaverde et al., 2004). The type and amount of dietary fat are important factors to consider, because vitamin E is fat-soluble. To our knowledge, there are no studies concerning the effect of different dietary fat inclusion levels upon -tocopherol absorption and deposition in poultry. The aim of this study was to assess the effect of different supplementation doses of -TA and of increasing levels of dietary unsaturated fat on apparent absorption and tissue deposition of -tocopherol in broiler chickens. |
MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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One hundred ninety-two Ross 308 female broiler chickens of 1 d of age were selected from a 2-fold larger population and distributed among pens to minimize variability in pen weight. The birds were housed in groups of 4 in 48 cages (width = 65 cm, length = 60 cm, and height = 40 cm) in a 3-level battery. Water was provided ad libitum by nipple drinkers. Temperature was kept initially at 29°C and was decreased 1°C every 3 d until 24 d of age, when it was maintained at 21°C. Birds were maintained on a photoperiod of 23:1.
The pens were randomly distributed into 16 dietary treatments of 3 replicates each. The 16 experimental treatments resulted from a 4 x4 factorial arrangement, where the 2 variation factors were the inclusion level of dietary fat and the inclusion level of vitamin E (-TA) in the diets. The 4 dietary fat inclusion levels were 2, 4, 6, and 8% (O2, O4, O6, and O8 treatments, respectively). The fat used was a mixture of linseed (Cailà & Parés, Barcelona, Spain) and fish oil (Agrupación de Fabricantes de Aceites Marinos, Barcelona, Spain) in a ratio of 4:1. Oils used in this trial were analyzed for moisture, impurities, unsaponifiable matter, acidity, and peroxide value to asses its quality at the start of the trial (Table 1
). The fat inclusion levels used (fat from ingredients + added fat) resulted in polyunsaturated fatty acid (PUFA) contents of 27, 38, 48, and 59 g/kg. All-rac--TA (Rovimix E-50 adsorbate, DSM, Barcelona, Spain) was added to the diets to obtain dietary -TA acetate concentrations of 0, 100, 200, and 400 mg/kg of feed. Measured -tocopherol concentrations are shown in Table 2.
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Feed and water were provided ad libitum. Feed samples were taken every 10 d during the experimental period for crude fat, total fatty acids, and -tocopherol determinations.
Sample Collection
Two digestibility balances were carried out at d 20 and 39 with the inclusion of Cr2O3 in the diets as a digestibility marker, to determine apparent absorption of organic matter, total fatty acids, and -tocopherol. A representative sample of excreta and feed was collected from each cage. The samples were freeze-dried, ground, and stored at –80°C until further analysis.
At the end of the experiment (40 d of age), half of the birds from each cage, selected by weight (6 birds per treatment), were transported to a commercial slaughterhouse, where they were killed and eviscerated. The livers of these birds were collected, freeze-dried, ground, and stored at –80°C until further analysis. From 48 of these birds (3 per treatment), a blood sample was collected in EDTA-coated tubes and immediately centrifuged to obtain the plasma fraction, which was frozen at –80°C until analysis. The other half of the birds was killed by lethal injection with sodium pentobarbitate (200 mg/kg), frozen, cut, and ground with a cutter (Tec-Maq model cut-20, INTEFISA, Barcelona, Spain), including feathers and blood. A representative sample was collected, freeze-dried, ground, and kept at –80°C until analysis.
Proximate Analyses of Diet and Excreta
Crude fat, crude fiber, CP, DM, and ash content were analyzed in the diet. Organic matter (OM) and crude fat content were analyzed in excreta. In all cases, the methodology of determination described in the AOAC (1995) was followed.
Diet AME was measured experimentally by the method of total excreta collection as explained in Villaverde et al. (2005). Gross energy was determined in feed and excreta by the means of an adiabatic bomb IKA-calorimeter C4000 (Staufen, Germany).
Chromium Analysis
Chromium concentration was measured in feed and excreta samples by atomic absorption following the procedure described by Williams et al. (1962).
-Tocopherol Analysis
Experimental Diets and Excreta.
-Tocopherol and -TA were determined following the method described by Lee et al. (1999) with modifications. Briefly, 100 mg of sample was mixed with water, 2-propanol, and extraction solvent [85% hexane (vol/vol); 15% ethyl acetate (vol/vol); 0.05% butylated hydroxytoluene (wt/vol)]. After homogenization and centrifugation, the organic layer was evaporated under stream of nitrogen, and the extract was rediluted in methanol and injected onto a reversed-phase HPLC column (Waters Spherisorb, Cerdanyola del Vallès, Spain) eluted with methanol (100%) and monitored with fluorescence detection (for -tocopherol) at 295/330 nm (excitation/emission) and ultraviolet detection (for -TA) at 284 nm. The 2 substances were identified comparing the retention times of -tocopherol and -TA standards (ref. T3251 and T3376, Sigma-Aldrich) and quantified by the means of a calibration curve and the use of phenyldodecane (ref. 44178, Sigma-Aldrich) as an internal standard, as described by Rupérez et al. (1999).
Liver and Whole Body.
-Tocopherol was extracted from liver and whole body as described previously by Surai et al. (1996) starting from 100 and 500 mg of freeze-dried sample, respectively.
Total Fatty Acid Determination
The total fatty acid (TFA) content of diets and excreta were determined by gas chromatography following the methodology described by Sukhija and Palmquist (1988), using nonadecanoic acid (C:19, ref. N5252, Sigma-Aldrich) as internal standard.
Calculations
To calculate the apparent absorption of vitamin E, the -TA values were transformed into -tocopherol equivalents (-TE; 1 mg of -TA is equivalent to 0.67 mg of TE). The apparent absorption of OM, fat, total fatty acids, and -TE was calculated as follows:
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The percentage of -TA hydrolysis into free -tocopherol was calculated in the same way:
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Statistics
Statistical analysis was carried out using the GLM procedure of SAS 9.1 (SAS institute Inc., Cary, NC), using dietary PUFA and -TA as classification factors. The interaction was also included in the model. The results of the 2 digestibility balances were analyzed separately, but the 2 balances were also compared including age in the model as a classification factor. Differences between treatment means were tested using Tukey’s correction for multiple comparisons. Alpha level used for the determination of significance in all comparisons was 0.05. Correlation between -tocopherol concentration in whole body, plasma, and liver were performed using the REG procedure of SAS 9.1. Regressions of hepatic -tocopherol content on dietary -tocopherol content for each diet varying in added fat and slope comparisons were performed using the GLM procedure of SAS 9.1 including the slope variable as a covariate.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Apparent Absorption of OM and TFA
Apparent absorption values of OM and TFA obtained in the 2 balance studies are shown in Table 3. Neither the TFA nor the OM apparent absorption coefficients were affected by the inclusion level of -TA. Organic matter apparent absorption was lower in the high-fat, high-PUFA diets, which also had a high percentage of crude fiber (P < 0.001). In all treatments, TFA apparent absorption was high (above 80%) and was increased with increasing oil inclusion level (P < 0.001). There were no differences between the 2 ages neither in OM (P = 0.502) nor in TFA (P = 0.937) apparent absorption, being the mean values 70.00 ± 0.44% and 87.79 ± 0.52%, respectively.
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-TE, -TA Hydrolysis, and Free Tocopherol Concentration in Excreta
Results of -TE apparent absorption coefficients are shown in Table 4. Due to the very low amounts of -tocopherol found in the excreta of the birds of the E0 treatments, these data were not considered accurate and hence are not presented in this table. Apparent absorption values on d 20 were higher than on d 39 (45.0 ± 1.75 vs. 50.1 ± 1.80; P = 0.001).
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-TA was significant (P = 0.002). In the O2 treatment, the apparent absorption value was lower in the birds supplemented with 100 mg/kg of -TA than in the birds supplemented with 200 (P = 0.003) and 400 (P = 0.013) mg/kg. In the older birds, neither dietary added fat nor dietary -TA affected apparent absorption values.
Average value for hydrolysis of -TA was 67.3 ± 3.00%. Dietary added PUFA-rich oil had no effect on this variable.
Nonesterified (Free) -Tocopherol Concentration in Excreta
Results are shown in Table 5. Both in the first and in the second balance study, the interaction between both dietary factors was significant. In all cases, increasing levels of dietary -TA resulted in a higher free -tocopherol concentration in excreta, but only at high levels of dietary -TA supplementation (E200 and E400) there were statistical differences depending on the level of added fat. In these treatments, higher fat inclusion levels (paralleled by higher PUFA inclusion levels) resulted in lower concentration of free -tocopherol excreted, and this happened in both ages.
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-Tocopherol Concentration
The concentration of -tocopherol in the whole body of the birds is presented in Table 6. There are clear differences in -tocopherol deposition in the whole body of chickens. The lower concentrations were found in the treatments with lower -TA supplementation but also in those treatments with high inclusion levels of PUFA-rich oil. The interaction between the 2 factors (P < 0.001) indicates that the differences in deposition due to -TA dietary supplementation are reduced in those birds fed high levels of added fat. Results concerning -tocopherol concentration in plasma and liver followed the same tendency as whole body -tocopherol (Tables 7 and 8).
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-tocopherol concentrations in whole body, liver, and plasma are presented in Table 9, and present correlation coefficients are above 0.85 in all cases. Regressions of hepatic -tocopherol content on dietary -tocopherol content for each fat level are presented
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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-tocopherol when compared with diets rich in saturated fat (tallow) at the same inclusion level. In the present experiment, in which the dietary fat used was always the same mixture of highly unsaturated oils (linseed and fish oils) but used at increasing levels, we have not found striking differences in apparent absorption between treatments; only in 20-d old birds we found a lower value for the O2, E100 treatment. There were no differences among treatments when birds were older.
Although it is accepted that dietary fat is necessary to a certain extent for the absorption of vitamin E, the minimum amount required for optimal absorption has not been determined in chickens. Regarding other species, the minimum amount of dietary fat in humans is being studied but has not been still established, and results are controversial. Some authors found no differences in vitamin E availability between high-fat or low-fat diets (Roodenburg et al., 2000), and other authors found that the amount of fat in a meal clearly influenced -tocopherol absorption (Jeanes et al., 2004). In rats, Brink et al. (1996) found no differences in -TE apparent absorption between a diet with 0.7 and 5.2% of added fat, and Losowsky et al. (1972) found no differences between diets containing 5 and 23% added fat. Our results suggest that 2% added fat (4.4% total dietary fat) is not limiting for a proper -tocopherol absorption in chickens, at least at the end of the growing phase. These results, however, may be different with the use of a more saturated dietary fat.
As to the effect of -TA supplementation dosage, our results are not conclusive. -Tocopheryl acetate dosage does not seem to have an effect upon -TE apparent absorption, except at 20 d of age in the birds fed the low-fat diet (O2), in which the birds supplemented with 100 mg/kg had lower apparent absorption values than the rest.
We can conclude that there is not a clear effect of -TA supplementation level upon -TE apparent absorption, which could be expected from the fact that -tocopherol is absorbed passively. Other authors found constant absorption values with increasing vitamin E supplementation (from 15 to 150 mg/d; Traber et al., 1998).
The previous step for -TE absorption is the hydrolysis of -TA into free -tocopherol. When feeding the birds with increasing levels of a PUFA-rich added fat, there were no clear differences among treatments in -TA hydrolysis percentage. However, the absorption values of
-TE coincide with the hydrolysis values of -TA at 20 d of age, being lower in the E100 treatment, and this could partly explain the low apparent absorption values of the birds fed the O2, E100 diet. We do not know the reason for this lower -TA hydrolysis under these conditions.
It has to be considered, though, that -tocopherol can be degraded before its absorption while protecting PUFA from oxidation in the gastrointestinal tract, as suggested by Tijburg et al. (1997). With the methodology used in this experiment, we cannot rule out this possibility, making it difficult to conclude that dietary PUFA inclusion enhances vitamin E absorption. However, the concentration of free -tocopherol in the excreta can be an indicator of gastrointestinal degradation.
Similarly, a high intake of PUFA can favor the appearance of peroxidation processes in the gut, as well as in the body tissues. Free -tocopherol concentration in the excreta is lower in the high-fat, high-PUFA treatments, and our results suggest a protective effect of -tocopherol in the gastrointestinal tract before its absorption. Sklan et al. (1982) suggested that at least 50% of the ingested tocopherol (administered as nonesterified -tocopherol) is degraded in the intestinal tract before absorption takes place. Interestingly, nonesterified -tocopherol concentration in excreta of the E0 and E100 treatments is not affected by dietary polyunsaturation.
Regarding vitamin E tissue concentration, the linear increase of -tocopherol concentration in chicken tissues with the increase in its dietary supplementation is well described (Jensen et al., 1999; Flachowsky et al., 2002). The -tocopherol concentration of liver increased with -TA supplementation, but the increase was lower in the high-PUFA treatments, despite the similar -TE apparent absorption coefficients among the different added fat treatments.
This interaction is similar to that found in the nonesterified -tocopherol concentration in the excreta. It has been suggested that there is -tocopherol recycling by other redox molecules such as ascorbate and glutathione (Surai, 1999). It is possible that the recycling is decreased when dietary -tocopherol supplementation is high.
We carried out linear regressions between dietary and hepatic -tocopherol concentration for each added fat treatment (O2, O4, O6, and O8, which have 28, 38, 48, and 59 g of PUFA/kg of diet). It can be observed that the slope of the equations is lower for the high-fat high-PUFA treatments. Given that the slope was not statistically different between O2 and O4 treatments, only an equation is presented.
These equations show that to achieve, for instance, 15 mg of -tocopherol/kg of fresh matter in liver it is necessary to provide 94, 150, and 214 mg/kg of -tocopherol in the diet if dietary PUFA are 28 to 38, 48, and 59 g/kg, respectively. That is, the ratio between dietary -tocopherol and PUFA to achieve the same -tocopherol concentration in chicken liver increases as PUFA does (2.47, 3.125, and 3.63 g/g, respectively, for previous examples).
The high-fat treatments are also richer in PUFA, and PUFA enrichment of tissues predisposes them to lipid peroxidation processes, in which vitamin E plays a protective role. Several authors have found that feeding diets rich in PUFA results in lower -tocopherol concentration in tissues, in rats (Tijburg et al., 1997), and in poultry (Ruiz et al., 1999; Surai and Sparks, 2000; Sijben et al., 2002). These results suggest that there is some -tocopherol destruction between absorption and deposition, or during deposition, due to the high-PUFA content of the high-fat diets, which would result in a high-PUFA deposition in the body. These results imply an important role of vitamin E in the increase of poultry meat shelf life when highly unsaturated diets are fed to these birds.
We measured -tocopherol not only in liver but also in the whole body and in plasma. We have found that whole body, liver, and plasma respond in a similar way to the experimental factors. This is expected, given that liver is considered a main -tocopherol depot tissue, and plasma is the means to transport -tocopherol to all body tissues. The good correlation between total and hepatic -tocopherol (r = 0.93) shows that -tocopherol concentration in liver is a useful indicator of total -tocopherol status in chickens. Correlation of both body and hepatic vitamin E with its concentration in plasma are good but somewhat lower (r = 0.91 and 0.87, respectively), probably due to the fact that -tocopherol is transported in plasma and deposited in the whole body and the liver. However, plasma -tocopherol showed the same differences among treatments and can also be considered a useful indicator of -tocopherol status in birds. The CV of these equations are too high to consider plasma and liver -tocopherol estimators of total body -tocopherol under our conditions. It is possible that the use of more samples can improve this CV. Plasma -tocopherol is the most used biomarker in mammals (especially humans) to assess -tocopherol status (Morrissey and Sheehy, 1999). Its advantages are that is noninvasive and is technically simple, but there are a high number of confounding factors (for example, age, sex, plasma lipids, smoking). The possibility of analyzing -tocopherol of the whole body of chickens allows us to confirm the usefulness of both hepatic and plasma -tocopherol in assessing the vitamin E status in chickens.
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REFERENCES |
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