Effect of Phaffia rhodozyma on performance, nutrient digestibility, blood characteristics, and meat quality in finishing pigs Y. Lei and I. H. Kim J ANIM SCI 2014, 92:171-176. doi: 10.2527/jas.2013-6749 originally published online December 18, 2013
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Effect of Phaffia rhodozyma on performance, nutrient digestibility, blood characteristics, and meat quality in finishing pigs Y. Lei* and I. H. Kim*1 *Department of Animal Resource and Science, Dankook University, Cheonan, Choongnam 330-714, South Korea
ABSTRACT: The red yeast, Phaffia rhodozyma (PR), has possible applications as a component of diets for use in the animal industry. Its primary value lies in its content of astaxanthin, which has been shown to be an antioxidant several times more effective than vitamin E. A total of 96 ([Landrace × Yorkshire] × Duroc) crossbred pigs with an initial BW of 58.61 ± 3.05 kg were used in this 10-wk feeding study to determine the effects of PR on growth performance, nutrient digestibility, blood characteristics, and meat quality in finishing pigs. Pigs were randomly allotted to 1 of 3 corn-soybean meal–based diets supplemented with 0, 0.1, or 0.2% PR. There were 8 replicate pens per treatment with 4 pigs (2 barrows and
2 gilts) per pen. The inclusion of PR linearly improved G:F in the phase 1 (P = 0.02), phase 2 (P = 0.02), and during the overall experimental period (P < 0.01) The DM digestibility was improved in the 0.1% PR treatment in phase 2 (quadratic, P = 0.01). The white blood cell concentration was increased in 0.1% PR group (P < 0.05) during phase 2 (quadratic, P < 0.01) and phase 2 (P = 0.04). The inclusion of graded levels of PR linearly increased (P < 0.01) the pH of LM. The 2-thiobarbituric acid reactive substances were linearly decreased (P = 0.03) by the supplementation of PR. In conclusion, the inclusion of PR could improve feed efficiency, DM digestibility, and meat quality of the finishing pig.
Key words: blood profile, finishing pig, meat quality, Phaffia rhodozyma © 2014 American Society of Animal Science. All rights reserved. J. Anim. Sci. 2014.92:171–176 doi:10.2527/jas2013-6749 INTRODUCTION Astaxanthin is a carotenoid that has potent antioxidative properties and exists naturally in various plants, algae, crustaceans, and seafood (Kurashige et al., 1990; Stahl and Sies, 2003). Storebakken and Goswami (1996) and Rehulka (2000) have suggested that astaxanthin is essential for the proper growth and survival of Atlantic salmon and rainbow trout. Lorenz and Cysewski (2000) reported that dietary inclusion of astaxanthin improved lean color and shelf life of farmed fish. Because of antioxidative and potential anti-inflammatory characteristics of astaxanthin, there is a growing interest in evaluating astaxanthin as a nutraceutical in domestic animal species. Previous research demonstrated that supplementation of the growing-finishing pig diet with vitamin E improved the pork quality because of its antioxidative function (Cannon et al., 1996). Astaxanthin is a
fat-soluble, red-colored carotenoid that has antioxidative properties several times more potent than vitamin E (Miki, 1991; Naguib, 2000). Yang et al. (2006) reported that dietary addition of 1.5 and 3 mg/kg of astaxanthin 14 d before slaughter linearly decreased the backfat depth and increased the carcass yield, as well as the LM area of finishing pigs. However, they did not observe any differences in measures of fresh pork color or quality. Therefore, we hypothesized that astaxanthin may have effects on pig meat quality when fed at higher levels. A red yeast, named Phaffia rhodozyma (PR), has been widely studied because of its capacity in producing astaxanthin (Montanti et al., 2011). However, little work has been done to evaluate the effects of astaxanthin supplementation on growth performance or meat quality in pigs. Therefore, the objective of the current study was to investigate the effect of PR supplementation on the performance, nutrient digestibility, blood characteristics, and meat quality of finishing pigs.
1Corresponding
author: [email protected] Received May 26, 2013. Accepted November 8, 2013.
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MATERIALS AND METHODS All pigs used in this trial were handled in accordance with the guidelines set forth by the Animal Care and Use Committee of Dankook University (Cheonan, Choongnam, South Korea). Experimental Design, Animals, and Diets A total of 96 ([Yorkshire× Landrace] × Duroc) crossbred pigs with an initial BW of 58.61 ± 3.05 kg were used in this 10-wk feeding study. Pigs were allotted to 1 of 3 treatments using a completely randomized design. There were 8 replicate pens per treatment with 4 pigs (2 barrows and 2 gilts) per pen. The experimental diets consisted of corn-soybean meal–based diets supplemented with 0, 0.1, or 0.2% PR. The PR was fermented in a jar and then freeze-dried, and the content of astaxanthin was 2,305 mg/kg (Sunbio Inc., Seongnam City, South Korea). All pigs were housed in an environmentally controlled room with a slatted plastic floor. Each pen (1.8 width × 1.8 m length) was equipped with a one-sided self-feeder and a nipple drinker to allow pigs ad libitum access to feed and water, respectively, throughout the experiment. All diets were formulated to meet or slightly exceed the nutrient requirements recommended by NRC (1998; Table 1). Experimental Procedures and Sampling Individual pig BW was recorded on d 0, 35, and 70 of the experiment, and feed consumption was recorded on a pen basis during the experiment to determine ADG, ADFI, and G:F. Chromic oxide was added to the diet (0.2%) for 5 d before the collection as an indigestible marker (Fenton and Fenton, 1979) to calculate the nutrient digestibility coefficient at the end of the 5th and 10th wk of the experiment. Chromium levels were determined via a UV absorption spectrophotometry (Shimadzu UV1201; Shimadzu, Kyoto, Japan) following the method described by Williams et al. (1962). Fresh fecal grab samples were obtained once daily from at least 2 pigs in each pen on the last 2 d of the 5th and 10th wk. After collection, all feed and fecal samples were stored immediately at -20°C until analysis. Before chemical analysis, diet and fecal samples were dried at 50°C for 72 h and finely ground to pass through a 1-mm screen, after which they were analyzed for DM (Method 930.15; AOAC, 1995), Ca (Method 984.01; AOAC, 1995), and P (Method 965.17; AOAC, 1995). Lysine was measured using an AA analyzer (Beckman 6300; Beckman Coulter, Inc., Fillerton, CA). Nitrogen was determined by a nitrogen analyzer (Kjectec 2300; Foss Tecator AB, Hoeganaes, Sweden). The GE was analyzed by an oxygen bomb calorimeter (Parr Instrument Co., Moline, IL).
Table 1. Composition of diets (as-fed basis)1 Level of PR (0 to 5 wk) Level of PR (6 to 10 wk) Item 0 0.1 0.2 0 0.1 0.2 Ingredient,% Corn 70.18 70.08 69.98 76.05 75.95 75.85 Soybean meal, 46.8% CP 22.16 22.16 22.16 16.40 16.40 16.40 Corn gluten 3.00 3.00 3.00 3.00 3.00 3.00 Tallow 2.76 2.76 2.76 2.20 2.20 2.20 Limestone 0.69 0.69 0.69 0.74 0.74 0.74 Salt 0.20 0.20 0.20 0.20 0.20 0.20 Dicalcium phosphate 0.66 0.66 0.66 1.10 1.10 1.10 Lysine 0.05 0.05 0.05 0.01 0.01 0.01 Vitamin premix2 0.20 0.20 0.20 0.20 0.20 0.20 Mineral premix3 0.10 0.10 0.10 0.10 0.10 0.10 PR 0.00 0.10 0.20 0.00 0.10 0.20 Calculated composition ME, kcal/kg 3,431 3,420 3,423 3,452 3,448 3,439 Analyzed composition, % CP 16.33 16.25 16.34 14.59 14.50 14.53 Lys 0.92 0.90 0.89 0.69 0.68 0.68 Ca 0.54 0.54 0.53 0.47 0.47 0.46 Total P 0.44 0.43 0.42 0.37 0.37 0.37 1PR = Phaffia rhodozyma, red yeast. 2Provided per kilogram of complete diet: 4000 IU of vitamin A, 800 IU of vitamin D3, 17 IU of vitamin E, 2.0 mg of vitamin K3, 4 mg of vitamin riboflavin, 1.0 mg of vitamin B6, 11 mg of pantothenic acid, 20.0 mg of niacin, and 0.02 mg of biotin. 3Provided per kilogram of complete diet: 12 mg of Cu as copper sulfate, 75 mg of Fe as ferrous sulfate, 56 mg of Zn as zinc oxide, 12.5 mg of Mn as manganese oxide, 0.3 mg of I as potassium iodate, and 0.15 mg of Se sodium selenite.
The apparent total tract digestibility of nutrients was calculated using the following formula according to Stein et al. (2006): digestibility (%) = {1 – [(Nf ×Cd)/ (Nd ×Cf)]} × 100, where Nf = nutrient concentration in feces (% DM), Nd = nutrient concentration in diet (% DM), Cf = chromium concentration in feces (% DM), and Cd = chromium concentration in diet (% DM). At the end of the 5th and 10th wk of the experiment, blood samples were collected from all pigs via jugular venipuncture. Blood samples were collected into K3EDTA vacuum tubes (Becton Dickinson Vacutainer Systems, Franklin Lakes, NJ) to evaluate blood characteristics. The white blood cell (WBC) and red blood cell (RBC) concentrations, as well as the lymphocytes percentage, were analyzed using an automatic blood analyzer (ADVIA 120; Bayer, New York, NY). At the end of the experiment, all pigs were slaughtered at a local commercial slaughter house. After chilling at 2°C for at least 24 h, a piece of the right loin was removed between the 10th and 11th ribs. Sensory evaluation (color, marbling, and firmness scores) was conducted according to the NPPC (1991) standards at an ambient temperature of 25°C. Immediately after the subjective tests were determined, the lightness (L*), redness (a*), and yellowness (b*) values were measured at 3 locations on the surface
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of each sample using a chroma meter (Model CR-410; Konica Minolta Sensing, Inc., Osaka, Japan). At the same time, duplicate pH values of each sample were directly measured using a pH Meter ( Model AR25, Fisher Scientific, Pittsburgh, PA). The water holding capacity (WHC) was measured in accordance with the methods described by Kauffman et al. (1986). Briefly, a 0.3-g sample was pressed at 3,000 psi for 3 min on a 125-mm-diameter piece of filter paper. The areas of the pressed sample and the expressed moisture were delineated and then determined using a sensor (Digitizing Area Line Sensor, MT-10S; M.T. Precision Co. Ltd., Tokyo, Japan). The ratio of water:meat area was calculated, giving a measure of WHC (a smaller ratio indicates increased WHC). The LM area was measured by tracing the LM surface at the 10th rib, which was determined using the aforementioned sensor. Drip loss was measured using approximately 4.5 g of meat sample according to the plastic bag method described by Honikel (1998). Cook loss was determined as described previously by Sullivan et al. (2007). The 2-thiobarbituric acid reactive substances (TBARS) were measured using the method described by Witte et al. (1970). The TBARS values were expressed in terms of milligrams of malonaldehyde (MDA) per kilogram of muscle. Trichloroacetic acid solution (20% wt/vol) was utilized for the extraction. The UV absorption spectrophotometry (UV-1201; Shimadzu) was used for the spectrophotometric analysis.
Table 2. Effect of graded levels of Phaffia rhodozyma (PR) on growth performance of finishing pigs Level of PR, % Item 0 0.1 Phase 1 (58 to 86 kg) ADG, kg/d 0.78 0.80 ADFI, kg/d 2.19 2.14 G:F 0.355 0.374 Phase 2 (86-114 kg) ADG, kg/d 0.89 0.92 ADFI, kg/d 2.88 2.84 G:F 0.309 0.322 Overall (58 to 114 kg) ADG, kg/d 0.83 0.86 ADFI, kg/d 2.53 2.49 G:F 0.329 0.344
P-value Linear Quadratic
0.2
SEM
0.79 2.07 0.381
0.05 0.07 0.007
0.58 0.06 0.02
0.27 0.88 0.49
0.90 2.81 0.321
0.04 0.09 0.003
0.27 0.29 0.02
0.13 0.95 0.11
0.85 2.44 0.346
0.02 0.03 0.003
0.33 0.06 < 0.01
0.13 0.95 0.14
No differences were observed in the RBC and lymphocyte levels among treatments (Table 4). The WBC concentration was enhanced in 0.1% PR group during phase 2 (quadratic, P < 0.01) and phase 2 (quadratic, P = 0.04). There was no difference in the meat color (L*, a*, b*values), sensory evaluation (color, firmness, and marbling), cooking loss, drip loss, LM area, and WHC among dietary treatments (Table 5). The inclusion of graded levels of PR linearly increased (P < 0.01) the pH of the LM. The TBARS was linearly decreased (P = 0.03) by PR supplementation. DISCUSSION
Statistical Analysis All data were analyzed using Mixed procedures of SAS (SAS Inst. Inc., Cary, NC).The model used was Yijk = μ + ti+ rk + eijk, where Yijk was an observation on the dependent variable ij; μ was the overall population mean; ti was the fixed effect of yeast addition treatments, rk was the pen as a random effect, and eijk was the random error associated with the observation ijk. Orthogonal polynomials were used to assess the linear and quadratic effects of increasing dietary concentrations of supplemental PR. RESULTS In this study, the inclusion of PR linearly improved feed efficiency in the phases 1 (P = 0.02) and 2 (P = 0.02) and the overall experimental period (P < 0.01; Table 2). The ADG and ADFI were not affected by increasing level of PR during the whole experimental period. There were no differences in N and the GE digestibility among all treatment groups throughout the experiment (Table 3). The DM digestibility was increased in the 0.1% PR treatment in phase 2 (quadratic, P = 0.01).
In this study, pigs fed the PR supplemented diets linearly increased G:F, but there was no effect on the ADG or ADFI. This is in agreement with Bergstrom et al. (2011), who demonstrated that pigs fed 30 or 60 mg/kg astaxanthin from Xanthophyllomyces dendrorhous had improved G:F. Inborr (1998) suggested that the inclusion of algae meal containing high astaxanthin led to a better G:F of poultry. However, Yang et al. (2006) found that Table 3. Effect of graded levels of Phaffia rhodozyma (PR) on apparent total tract nutrient digestibility of finishing pigs Item 0 Phase 1 (58 to 86 kg) DM 76.31 N 76.42 Energy 76.18 Phase 2 (86 to 114 kg) DM 70.87 N 73.33 Energy 73.33
Level of PR, % 0.1 0.2
SEM
P-value Linear Quadratic
76.80 76.79 76.53
77.33 77.75 76.41
0.94 1.49 1.05
0.49 0.30 0.48
0.56 0.57 0.62
74.65 75.06 74.33
73.68 74.48 74.09
1.15 1.13 1.37
0.06 0.06 0.17
0.01 0.07 0.24
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Table 4. Effect of graded levels of Phaffia rhodozyma (PR) on blood profiles of finishing pigs1 Level of PR, % Item 0 0.1 0.2 Phase 1 (58 to 86 kg) RBC, 106/µL 6.97 7.07 6.93 22.27 19.52 WBC, 103/µL 16.47 Lymphocyte, % 62.2 60.3 59.9 Phase 2 (86 to 114 kg) RBC, 106/µL 7.45 7.28 7.55 WBC, 103/µL 16.39 18.34 17.18 Lymphocyte, % 70.2 67.3 65.9 1RBC
SEM
P-value Linear Quadratic
0.11 1.02 2.21
0.80 0.06 0.24
0.43 < 0.01 0.26
0.15 0.54 1.57
0.64 0.33 0.08
0.27 0.04 0.70
= red blood cell; and WBC = white blood cell.
there was no effect on the finishing pig performance by the administration of 1.5 and 3 mg/kg astaxanthin. Akiba et al. (2001) reported that the inclusion of PR did not affect the performance of broilers compared with those fed the control diet. The reason for the different results in the aforementioned studies may be attributed to the different experiment conditions, animals, and different dosages and sources of PR. On the other hand, we found a greater DM digestibility in the PR treatment, which may be relevant to the increased G:F observed in the current study. As we all know, WBCs are very important to the immune system. In the current study, we found that the WBC concentration was increased by the addition of PR. A large number of studies have shown that astaxanthin improves the immune function (Kim et al., 2000; Park et al., 2010). There might be 2 reasons for the immune regulation function of astaxanthin. First, Astaxanthin can stimulate the cell proliferation of murine splenocytes, thymocytes, and some other immunerelated cells (Okai and Higashi-Okai, 1996; Park et al., 2010). In addition, immune cells are particularly sensitive to membrane damage by free radicals (Chew and Park, 2004). Astaxanthin, which exerted excellent antioxidative activity could protect immune cells from oxidative injury. However, Chew et al. (2011) indicated that the addition of 10, 20, or 40 mg/d astaxanthin did not affect the number of WBCs in dogs. This inconsistency may be due to the different animal species. The TBARS is a frequently used method for measurement of lipid oxidation. The lower the TBARS value, the less oxidation has taken place (Yang et al., 2006). In the present study, inclusion of astaxanthin decreased the TBARS values. An et al. (2004) found that the production of lipid peroxides in the carcasses of broiler chickens during storage could be delayed by astaxanthin. Yang et al. (2006) also suggested that the TBARS value decreased with the increased astaxanthin addition. The reason for this effect is possibly due to the improved lipid stability because of the beneficial effect of astaxanthin on superoxide dismutase, catalase, and glutathione
Table 5. Effect of graded levels of Phaffia rhodozyma (PR) on meat quality of finishing pigs1 Item Meat color L* a* b* Sensory evaluation Color Firmness Marbling Cooking loss, % Drip loss,% d1 d3 d5 d7 pH LM area, cm2 Water holding capacity, % TBARS, mg MDA/kg
0
Level of PR , % 0.1 0.2
P-value SEM Linear Quadratic
57.44 17.47 10.60
58.63 17.62 10.48
57.28 16.75 10.82
0.69 0.34 0.51
0.87 0.16 0.76
0.15 0.25 0.72
1.93 1.89 1.97 30.28
1.99 1.95 1.98 28.85
2.00 1.99 2.06 30.04
0.04 0.04 0.08 0.81
0.27 0.10 0.42 0.84
0.66 0.88 0.69 0.21
8.21 12.51 14.26 16.01 5.35 48.30 57.38 0.023
9.46 13.21 13.70 15.31 5.42 49.52 58.80 0.020
8.71 12.42 13.86 16.22 5.51 48.67 58.27 0.019
1.60 0.83 1.55 0.97 1.31 0.93 1.27 0.90 0.03 < 0.01 0.92 0.78 1.97 0.75 0.001 0.03
0.62 0.70 0.82 0.61 0.90 0.37 0.69 0.15
1TBARS = thiobarbituric acid reactive substance; and MDA = malondialdehyde.
peroxidase activities (Kobayashi et al., 1997; Kurashige et al., 1990). Santos and Mesquita (1984) showed that astaxanthin located in cytosolic lipid globules and membraneous regions of cysts could make up for the lack of those enzymes and antioxidants. Furthermore, Krinsky (1989) showed that astaxanthin can prevent oxidative injury to cyst cells caused by exposure to reactive oxygen species generated by methyl viologen. Therefore, astaxanthin might act as an antioxidant by reacting with active oxygen radicals, providing antioxidative protection in the cytoplasm and in lipid membranes. This explains the increased immune cell, WBC, in our study. Astaxanthin is a fat-soluble, red-colored carotenoid, which is used as a pigment in the animal industry (Bjerkeng et al., 2007). However, previous study showed that dietary addition of 1.5 and 3 mg/kg of astaxanthin could not affect the meat quality of finishing pigs (Yang et al., 2006). In the present study, we also found that the meat color was not affected by the greater supplementation of astaxanthin. Similarly, Carr et al. (2010) also showed that even 66.7 mg/kg astaxanthin supplementation had no effect on pork color. In contrast, dietary supplementation with 0.675 mg/kg and 0.242 mg/kg astaxanthin resulted in redder meat in broilers (Akiba et al., 2001; An et al., 2004) and darker egg yolks in laying hens (Akiba et al., 2000). The 0.1 mg/kg astaxanthin also can lead to a redder meat of crustaceans (Chien and Jeng, 1992). This discrepancy may be due to the species. Much greater dosages may be needed in pigs. Therefore, the effect of astaxanthin on the pork color requires further investigation.
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Phaffia rhodozyma in finishing pigs
Meat pH is another characteristic of meat quality and affects the water holding capacity of meat (Gou et al., 2002). In our study, we found that the supplementation of PR increased the pH of the meat. However, Carr et al. (2010) indicated that astaxanthin could not affect the pH of the pork. To the best of our knowledge, there is relatively limited data on the effect of astaxanthin supplementation on pigs, and further studies will be necessary to evaluate the effects of astaxanthin on meat pH. In conclusion, the inclusion of PR improved G:F and DM digestibility. The pH of the meat was enhanced and the TBARS was decreased with the supplementation of PR in the finishing pig. The PR could be a good resource to supply the astaxanthin, which can improve G:F, immunity status, and meat quality of the finishing pigs. LITERATURE CITED Akiba, Y., K. Sato, K. Takahashi, M. Toyomizu, Y. Takahashi, S. Konashi, H. Nishida, H. Tsunekawa, Y. Hayasaka, and H. Nagao. 2000. Improved pigmentation of egg yolk by feeding of yeast Phaffia rhodozyma containing high concentration of astaxanthin in laying hens. Jpn. Poult. Sci. 37:162–170. Akiba, Y., K. Sato, K. Takahashi, K. Matsushita, H. Komiyama, H. Tsunekawa, and H. Nagao. 2001. Meat color modification in broiler chickens by feeding yeast Phaffia rhodozyma containing high concentrations of astaxanthin. J. Appl. Poult. Res. 10:154–161. An, G. H., J. H. Song, K. S. Chang, B. D. Lee, H. S. Chae, and B. G. Jang. 2004. Pigmentation and delayed oxidation of broiler chickens by the red carotenoid, astaxanthin, from chemical synthesis and the yeast Xanthophyllomyces dendrorhous. AsianAustralas. J. Anim. Sci. 17:1309–1314. AOAC. 1995. Official method of analysis. 16th ed. Assoc. Off. Anal. Chem., Washington, DC. Bergstrom, J. R., G. R. Skaar, T. A. Houser, M. D. Tokach, S. S. Dritz, J. L. Nelssen, R. D. Goodband, and J. M. DeRouchey. 2011. Effects of dietary astaxanthin and ractopamine HCl on the growth and carcass characteristics of finishing pigs and the color shelf-life of longissimus chops from barrows and gilts. In: Proc. Swine Day, Univ. of Kansas, Manhattan. p. 330–340. Bjerkeng, B., M. Peisker, K. von Schwartzenberg, T. Ytrestoyl, and T. Asgard. 2007. Digestibility and muscle retention of astaxanthin in Atlantic salmon, Salmo salar, fed diets with the red yeast Phaffia rhodozyma in comparison with synthetic formulated astaxanthin. Aquaculture 269:476–489. Cannon, J. E., J. B. Morgan, G. R. Schmidt, J.D. Tatum, J. N. Sofos, G. C. Smith, R. J. Delmore, and S. N. Williams. 1996. Growth and fresh meat quality characteristics of pigs supplemented with vitamin E. J. Anim. Sci. 74:98–105. Carr, C. C., D. D. Johnson, J. H. Brendemuhl, and J. M. Gonzalez. 2010. Fresh pork quality and shelf-life characteristics of meat from pigs supplemented with natural astaxanthin in the diet. Prof. Anim. Sci. 26:18–25. Chien, Y. H., and S. C. Jeng. 1992. Pigmentation of kuruma prawn, Penaeus japonicus Bate, by various pigment sources and levels and feeding regimes. Aquaculture 102:333–346. Chew, B. P., B. D. Mathison, M. G. Hayek, S. Massimino, G. A. Reinhart, and J. S. Park. 2011. Dietary astaxanthin enhances immune response in dogs. Vet. Immunol. Immunopathol. 140:199–206.
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Effect of Phaffia rhodozyma on performance, nutrient digestibility, blood characteristics, and meat quality in finishing pigs Y. Lei* and I. H. Kim*1 *Department of Animal Resource and Science, Dankook University, Cheonan, Choongnam 330-714, South Korea
ABSTRACT: The red yeast, Phaffia rhodozyma (PR), has possible applications as a component of diets for use in the animal industry. Its primary value lies in its content of astaxanthin, which has been shown to be an antioxidant several times more effective than vitamin E. A total of 96 ([Landrace × Yorkshire] × Duroc) crossbred pigs with an initial BW of 58.61 ± 3.05 kg were used in this 10-wk feeding study to determine the effects of PR on growth performance, nutrient digestibility, blood characteristics, and meat quality in finishing pigs. Pigs were randomly allotted to 1 of 3 corn-soybean meal–based diets supplemented with 0, 0.1, or 0.2% PR. There were 8 replicate pens per treatment with 4 pigs (2 barrows and
2 gilts) per pen. The inclusion of PR linearly improved G:F in the phase 1 (P = 0.02), phase 2 (P = 0.02), and during the overall experimental period (P < 0.01) The DM digestibility was improved in the 0.1% PR treatment in phase 2 (quadratic, P = 0.01). The white blood cell concentration was increased in 0.1% PR group (P < 0.05) during phase 2 (quadratic, P < 0.01) and phase 2 (P = 0.04). The inclusion of graded levels of PR linearly increased (P < 0.01) the pH of LM. The 2-thiobarbituric acid reactive substances were linearly decreased (P = 0.03) by the supplementation of PR. In conclusion, the inclusion of PR could improve feed efficiency, DM digestibility, and meat quality of the finishing pig.
Key words: blood profile, finishing pig, meat quality, Phaffia rhodozyma © 2014 American Society of Animal Science. All rights reserved. J. Anim. Sci. 2014.92:171–176 doi:10.2527/jas2013-6749 INTRODUCTION Astaxanthin is a carotenoid that has potent antioxidative properties and exists naturally in various plants, algae, crustaceans, and seafood (Kurashige et al., 1990; Stahl and Sies, 2003). Storebakken and Goswami (1996) and Rehulka (2000) have suggested that astaxanthin is essential for the proper growth and survival of Atlantic salmon and rainbow trout. Lorenz and Cysewski (2000) reported that dietary inclusion of astaxanthin improved lean color and shelf life of farmed fish. Because of antioxidative and potential anti-inflammatory characteristics of astaxanthin, there is a growing interest in evaluating astaxanthin as a nutraceutical in domestic animal species. Previous research demonstrated that supplementation of the growing-finishing pig diet with vitamin E improved the pork quality because of its antioxidative function (Cannon et al., 1996). Astaxanthin is a
fat-soluble, red-colored carotenoid that has antioxidative properties several times more potent than vitamin E (Miki, 1991; Naguib, 2000). Yang et al. (2006) reported that dietary addition of 1.5 and 3 mg/kg of astaxanthin 14 d before slaughter linearly decreased the backfat depth and increased the carcass yield, as well as the LM area of finishing pigs. However, they did not observe any differences in measures of fresh pork color or quality. Therefore, we hypothesized that astaxanthin may have effects on pig meat quality when fed at higher levels. A red yeast, named Phaffia rhodozyma (PR), has been widely studied because of its capacity in producing astaxanthin (Montanti et al., 2011). However, little work has been done to evaluate the effects of astaxanthin supplementation on growth performance or meat quality in pigs. Therefore, the objective of the current study was to investigate the effect of PR supplementation on the performance, nutrient digestibility, blood characteristics, and meat quality of finishing pigs.
1Corresponding
author: [email protected] Received May 26, 2013. Accepted November 8, 2013.
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MATERIALS AND METHODS All pigs used in this trial were handled in accordance with the guidelines set forth by the Animal Care and Use Committee of Dankook University (Cheonan, Choongnam, South Korea). Experimental Design, Animals, and Diets A total of 96 ([Yorkshire× Landrace] × Duroc) crossbred pigs with an initial BW of 58.61 ± 3.05 kg were used in this 10-wk feeding study. Pigs were allotted to 1 of 3 treatments using a completely randomized design. There were 8 replicate pens per treatment with 4 pigs (2 barrows and 2 gilts) per pen. The experimental diets consisted of corn-soybean meal–based diets supplemented with 0, 0.1, or 0.2% PR. The PR was fermented in a jar and then freeze-dried, and the content of astaxanthin was 2,305 mg/kg (Sunbio Inc., Seongnam City, South Korea). All pigs were housed in an environmentally controlled room with a slatted plastic floor. Each pen (1.8 width × 1.8 m length) was equipped with a one-sided self-feeder and a nipple drinker to allow pigs ad libitum access to feed and water, respectively, throughout the experiment. All diets were formulated to meet or slightly exceed the nutrient requirements recommended by NRC (1998; Table 1). Experimental Procedures and Sampling Individual pig BW was recorded on d 0, 35, and 70 of the experiment, and feed consumption was recorded on a pen basis during the experiment to determine ADG, ADFI, and G:F. Chromic oxide was added to the diet (0.2%) for 5 d before the collection as an indigestible marker (Fenton and Fenton, 1979) to calculate the nutrient digestibility coefficient at the end of the 5th and 10th wk of the experiment. Chromium levels were determined via a UV absorption spectrophotometry (Shimadzu UV1201; Shimadzu, Kyoto, Japan) following the method described by Williams et al. (1962). Fresh fecal grab samples were obtained once daily from at least 2 pigs in each pen on the last 2 d of the 5th and 10th wk. After collection, all feed and fecal samples were stored immediately at -20°C until analysis. Before chemical analysis, diet and fecal samples were dried at 50°C for 72 h and finely ground to pass through a 1-mm screen, after which they were analyzed for DM (Method 930.15; AOAC, 1995), Ca (Method 984.01; AOAC, 1995), and P (Method 965.17; AOAC, 1995). Lysine was measured using an AA analyzer (Beckman 6300; Beckman Coulter, Inc., Fillerton, CA). Nitrogen was determined by a nitrogen analyzer (Kjectec 2300; Foss Tecator AB, Hoeganaes, Sweden). The GE was analyzed by an oxygen bomb calorimeter (Parr Instrument Co., Moline, IL).
Table 1. Composition of diets (as-fed basis)1 Level of PR (0 to 5 wk) Level of PR (6 to 10 wk) Item 0 0.1 0.2 0 0.1 0.2 Ingredient,% Corn 70.18 70.08 69.98 76.05 75.95 75.85 Soybean meal, 46.8% CP 22.16 22.16 22.16 16.40 16.40 16.40 Corn gluten 3.00 3.00 3.00 3.00 3.00 3.00 Tallow 2.76 2.76 2.76 2.20 2.20 2.20 Limestone 0.69 0.69 0.69 0.74 0.74 0.74 Salt 0.20 0.20 0.20 0.20 0.20 0.20 Dicalcium phosphate 0.66 0.66 0.66 1.10 1.10 1.10 Lysine 0.05 0.05 0.05 0.01 0.01 0.01 Vitamin premix2 0.20 0.20 0.20 0.20 0.20 0.20 Mineral premix3 0.10 0.10 0.10 0.10 0.10 0.10 PR 0.00 0.10 0.20 0.00 0.10 0.20 Calculated composition ME, kcal/kg 3,431 3,420 3,423 3,452 3,448 3,439 Analyzed composition, % CP 16.33 16.25 16.34 14.59 14.50 14.53 Lys 0.92 0.90 0.89 0.69 0.68 0.68 Ca 0.54 0.54 0.53 0.47 0.47 0.46 Total P 0.44 0.43 0.42 0.37 0.37 0.37 1PR = Phaffia rhodozyma, red yeast. 2Provided per kilogram of complete diet: 4000 IU of vitamin A, 800 IU of vitamin D3, 17 IU of vitamin E, 2.0 mg of vitamin K3, 4 mg of vitamin riboflavin, 1.0 mg of vitamin B6, 11 mg of pantothenic acid, 20.0 mg of niacin, and 0.02 mg of biotin. 3Provided per kilogram of complete diet: 12 mg of Cu as copper sulfate, 75 mg of Fe as ferrous sulfate, 56 mg of Zn as zinc oxide, 12.5 mg of Mn as manganese oxide, 0.3 mg of I as potassium iodate, and 0.15 mg of Se sodium selenite.
The apparent total tract digestibility of nutrients was calculated using the following formula according to Stein et al. (2006): digestibility (%) = {1 – [(Nf ×Cd)/ (Nd ×Cf)]} × 100, where Nf = nutrient concentration in feces (% DM), Nd = nutrient concentration in diet (% DM), Cf = chromium concentration in feces (% DM), and Cd = chromium concentration in diet (% DM). At the end of the 5th and 10th wk of the experiment, blood samples were collected from all pigs via jugular venipuncture. Blood samples were collected into K3EDTA vacuum tubes (Becton Dickinson Vacutainer Systems, Franklin Lakes, NJ) to evaluate blood characteristics. The white blood cell (WBC) and red blood cell (RBC) concentrations, as well as the lymphocytes percentage, were analyzed using an automatic blood analyzer (ADVIA 120; Bayer, New York, NY). At the end of the experiment, all pigs were slaughtered at a local commercial slaughter house. After chilling at 2°C for at least 24 h, a piece of the right loin was removed between the 10th and 11th ribs. Sensory evaluation (color, marbling, and firmness scores) was conducted according to the NPPC (1991) standards at an ambient temperature of 25°C. Immediately after the subjective tests were determined, the lightness (L*), redness (a*), and yellowness (b*) values were measured at 3 locations on the surface
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of each sample using a chroma meter (Model CR-410; Konica Minolta Sensing, Inc., Osaka, Japan). At the same time, duplicate pH values of each sample were directly measured using a pH Meter ( Model AR25, Fisher Scientific, Pittsburgh, PA). The water holding capacity (WHC) was measured in accordance with the methods described by Kauffman et al. (1986). Briefly, a 0.3-g sample was pressed at 3,000 psi for 3 min on a 125-mm-diameter piece of filter paper. The areas of the pressed sample and the expressed moisture were delineated and then determined using a sensor (Digitizing Area Line Sensor, MT-10S; M.T. Precision Co. Ltd., Tokyo, Japan). The ratio of water:meat area was calculated, giving a measure of WHC (a smaller ratio indicates increased WHC). The LM area was measured by tracing the LM surface at the 10th rib, which was determined using the aforementioned sensor. Drip loss was measured using approximately 4.5 g of meat sample according to the plastic bag method described by Honikel (1998). Cook loss was determined as described previously by Sullivan et al. (2007). The 2-thiobarbituric acid reactive substances (TBARS) were measured using the method described by Witte et al. (1970). The TBARS values were expressed in terms of milligrams of malonaldehyde (MDA) per kilogram of muscle. Trichloroacetic acid solution (20% wt/vol) was utilized for the extraction. The UV absorption spectrophotometry (UV-1201; Shimadzu) was used for the spectrophotometric analysis.
Table 2. Effect of graded levels of Phaffia rhodozyma (PR) on growth performance of finishing pigs Level of PR, % Item 0 0.1 Phase 1 (58 to 86 kg) ADG, kg/d 0.78 0.80 ADFI, kg/d 2.19 2.14 G:F 0.355 0.374 Phase 2 (86-114 kg) ADG, kg/d 0.89 0.92 ADFI, kg/d 2.88 2.84 G:F 0.309 0.322 Overall (58 to 114 kg) ADG, kg/d 0.83 0.86 ADFI, kg/d 2.53 2.49 G:F 0.329 0.344
P-value Linear Quadratic
0.2
SEM
0.79 2.07 0.381
0.05 0.07 0.007
0.58 0.06 0.02
0.27 0.88 0.49
0.90 2.81 0.321
0.04 0.09 0.003
0.27 0.29 0.02
0.13 0.95 0.11
0.85 2.44 0.346
0.02 0.03 0.003
0.33 0.06 < 0.01
0.13 0.95 0.14
No differences were observed in the RBC and lymphocyte levels among treatments (Table 4). The WBC concentration was enhanced in 0.1% PR group during phase 2 (quadratic, P < 0.01) and phase 2 (quadratic, P = 0.04). There was no difference in the meat color (L*, a*, b*values), sensory evaluation (color, firmness, and marbling), cooking loss, drip loss, LM area, and WHC among dietary treatments (Table 5). The inclusion of graded levels of PR linearly increased (P < 0.01) the pH of the LM. The TBARS was linearly decreased (P = 0.03) by PR supplementation. DISCUSSION
Statistical Analysis All data were analyzed using Mixed procedures of SAS (SAS Inst. Inc., Cary, NC).The model used was Yijk = μ + ti+ rk + eijk, where Yijk was an observation on the dependent variable ij; μ was the overall population mean; ti was the fixed effect of yeast addition treatments, rk was the pen as a random effect, and eijk was the random error associated with the observation ijk. Orthogonal polynomials were used to assess the linear and quadratic effects of increasing dietary concentrations of supplemental PR. RESULTS In this study, the inclusion of PR linearly improved feed efficiency in the phases 1 (P = 0.02) and 2 (P = 0.02) and the overall experimental period (P < 0.01; Table 2). The ADG and ADFI were not affected by increasing level of PR during the whole experimental period. There were no differences in N and the GE digestibility among all treatment groups throughout the experiment (Table 3). The DM digestibility was increased in the 0.1% PR treatment in phase 2 (quadratic, P = 0.01).
In this study, pigs fed the PR supplemented diets linearly increased G:F, but there was no effect on the ADG or ADFI. This is in agreement with Bergstrom et al. (2011), who demonstrated that pigs fed 30 or 60 mg/kg astaxanthin from Xanthophyllomyces dendrorhous had improved G:F. Inborr (1998) suggested that the inclusion of algae meal containing high astaxanthin led to a better G:F of poultry. However, Yang et al. (2006) found that Table 3. Effect of graded levels of Phaffia rhodozyma (PR) on apparent total tract nutrient digestibility of finishing pigs Item 0 Phase 1 (58 to 86 kg) DM 76.31 N 76.42 Energy 76.18 Phase 2 (86 to 114 kg) DM 70.87 N 73.33 Energy 73.33
Level of PR, % 0.1 0.2
SEM
P-value Linear Quadratic
76.80 76.79 76.53
77.33 77.75 76.41
0.94 1.49 1.05
0.49 0.30 0.48
0.56 0.57 0.62
74.65 75.06 74.33
73.68 74.48 74.09
1.15 1.13 1.37
0.06 0.06 0.17
0.01 0.07 0.24
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Table 4. Effect of graded levels of Phaffia rhodozyma (PR) on blood profiles of finishing pigs1 Level of PR, % Item 0 0.1 0.2 Phase 1 (58 to 86 kg) RBC, 106/µL 6.97 7.07 6.93 22.27 19.52 WBC, 103/µL 16.47 Lymphocyte, % 62.2 60.3 59.9 Phase 2 (86 to 114 kg) RBC, 106/µL 7.45 7.28 7.55 WBC, 103/µL 16.39 18.34 17.18 Lymphocyte, % 70.2 67.3 65.9 1RBC
SEM
P-value Linear Quadratic
0.11 1.02 2.21
0.80 0.06 0.24
0.43 < 0.01 0.26
0.15 0.54 1.57
0.64 0.33 0.08
0.27 0.04 0.70
= red blood cell; and WBC = white blood cell.
there was no effect on the finishing pig performance by the administration of 1.5 and 3 mg/kg astaxanthin. Akiba et al. (2001) reported that the inclusion of PR did not affect the performance of broilers compared with those fed the control diet. The reason for the different results in the aforementioned studies may be attributed to the different experiment conditions, animals, and different dosages and sources of PR. On the other hand, we found a greater DM digestibility in the PR treatment, which may be relevant to the increased G:F observed in the current study. As we all know, WBCs are very important to the immune system. In the current study, we found that the WBC concentration was increased by the addition of PR. A large number of studies have shown that astaxanthin improves the immune function (Kim et al., 2000; Park et al., 2010). There might be 2 reasons for the immune regulation function of astaxanthin. First, Astaxanthin can stimulate the cell proliferation of murine splenocytes, thymocytes, and some other immunerelated cells (Okai and Higashi-Okai, 1996; Park et al., 2010). In addition, immune cells are particularly sensitive to membrane damage by free radicals (Chew and Park, 2004). Astaxanthin, which exerted excellent antioxidative activity could protect immune cells from oxidative injury. However, Chew et al. (2011) indicated that the addition of 10, 20, or 40 mg/d astaxanthin did not affect the number of WBCs in dogs. This inconsistency may be due to the different animal species. The TBARS is a frequently used method for measurement of lipid oxidation. The lower the TBARS value, the less oxidation has taken place (Yang et al., 2006). In the present study, inclusion of astaxanthin decreased the TBARS values. An et al. (2004) found that the production of lipid peroxides in the carcasses of broiler chickens during storage could be delayed by astaxanthin. Yang et al. (2006) also suggested that the TBARS value decreased with the increased astaxanthin addition. The reason for this effect is possibly due to the improved lipid stability because of the beneficial effect of astaxanthin on superoxide dismutase, catalase, and glutathione
Table 5. Effect of graded levels of Phaffia rhodozyma (PR) on meat quality of finishing pigs1 Item Meat color L* a* b* Sensory evaluation Color Firmness Marbling Cooking loss, % Drip loss,% d1 d3 d5 d7 pH LM area, cm2 Water holding capacity, % TBARS, mg MDA/kg
0
Level of PR , % 0.1 0.2
P-value SEM Linear Quadratic
57.44 17.47 10.60
58.63 17.62 10.48
57.28 16.75 10.82
0.69 0.34 0.51
0.87 0.16 0.76
0.15 0.25 0.72
1.93 1.89 1.97 30.28
1.99 1.95 1.98 28.85
2.00 1.99 2.06 30.04
0.04 0.04 0.08 0.81
0.27 0.10 0.42 0.84
0.66 0.88 0.69 0.21
8.21 12.51 14.26 16.01 5.35 48.30 57.38 0.023
9.46 13.21 13.70 15.31 5.42 49.52 58.80 0.020
8.71 12.42 13.86 16.22 5.51 48.67 58.27 0.019
1.60 0.83 1.55 0.97 1.31 0.93 1.27 0.90 0.03 < 0.01 0.92 0.78 1.97 0.75 0.001 0.03
0.62 0.70 0.82 0.61 0.90 0.37 0.69 0.15
1TBARS = thiobarbituric acid reactive substance; and MDA = malondialdehyde.
peroxidase activities (Kobayashi et al., 1997; Kurashige et al., 1990). Santos and Mesquita (1984) showed that astaxanthin located in cytosolic lipid globules and membraneous regions of cysts could make up for the lack of those enzymes and antioxidants. Furthermore, Krinsky (1989) showed that astaxanthin can prevent oxidative injury to cyst cells caused by exposure to reactive oxygen species generated by methyl viologen. Therefore, astaxanthin might act as an antioxidant by reacting with active oxygen radicals, providing antioxidative protection in the cytoplasm and in lipid membranes. This explains the increased immune cell, WBC, in our study. Astaxanthin is a fat-soluble, red-colored carotenoid, which is used as a pigment in the animal industry (Bjerkeng et al., 2007). However, previous study showed that dietary addition of 1.5 and 3 mg/kg of astaxanthin could not affect the meat quality of finishing pigs (Yang et al., 2006). In the present study, we also found that the meat color was not affected by the greater supplementation of astaxanthin. Similarly, Carr et al. (2010) also showed that even 66.7 mg/kg astaxanthin supplementation had no effect on pork color. In contrast, dietary supplementation with 0.675 mg/kg and 0.242 mg/kg astaxanthin resulted in redder meat in broilers (Akiba et al., 2001; An et al., 2004) and darker egg yolks in laying hens (Akiba et al., 2000). The 0.1 mg/kg astaxanthin also can lead to a redder meat of crustaceans (Chien and Jeng, 1992). This discrepancy may be due to the species. Much greater dosages may be needed in pigs. Therefore, the effect of astaxanthin on the pork color requires further investigation.
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Meat pH is another characteristic of meat quality and affects the water holding capacity of meat (Gou et al., 2002). In our study, we found that the supplementation of PR increased the pH of the meat. However, Carr et al. (2010) indicated that astaxanthin could not affect the pH of the pork. To the best of our knowledge, there is relatively limited data on the effect of astaxanthin supplementation on pigs, and further studies will be necessary to evaluate the effects of astaxanthin on meat pH. In conclusion, the inclusion of PR improved G:F and DM digestibility. The pH of the meat was enhanced and the TBARS was decreased with the supplementation of PR in the finishing pig. The PR could be a good resource to supply the astaxanthin, which can improve G:F, immunity status, and meat quality of the finishing pigs. LITERATURE CITED Akiba, Y., K. Sato, K. Takahashi, M. Toyomizu, Y. Takahashi, S. Konashi, H. Nishida, H. Tsunekawa, Y. Hayasaka, and H. Nagao. 2000. Improved pigmentation of egg yolk by feeding of yeast Phaffia rhodozyma containing high concentration of astaxanthin in laying hens. Jpn. Poult. Sci. 37:162–170. Akiba, Y., K. Sato, K. Takahashi, K. Matsushita, H. Komiyama, H. Tsunekawa, and H. Nagao. 2001. Meat color modification in broiler chickens by feeding yeast Phaffia rhodozyma containing high concentrations of astaxanthin. J. Appl. Poult. Res. 10:154–161. An, G. H., J. H. Song, K. S. Chang, B. D. Lee, H. S. Chae, and B. G. Jang. 2004. Pigmentation and delayed oxidation of broiler chickens by the red carotenoid, astaxanthin, from chemical synthesis and the yeast Xanthophyllomyces dendrorhous. AsianAustralas. J. Anim. Sci. 17:1309–1314. AOAC. 1995. Official method of analysis. 16th ed. Assoc. Off. Anal. Chem., Washington, DC. Bergstrom, J. R., G. R. Skaar, T. A. Houser, M. D. Tokach, S. S. Dritz, J. L. Nelssen, R. D. Goodband, and J. M. DeRouchey. 2011. Effects of dietary astaxanthin and ractopamine HCl on the growth and carcass characteristics of finishing pigs and the color shelf-life of longissimus chops from barrows and gilts. In: Proc. Swine Day, Univ. of Kansas, Manhattan. p. 330–340. Bjerkeng, B., M. Peisker, K. von Schwartzenberg, T. Ytrestoyl, and T. Asgard. 2007. Digestibility and muscle retention of astaxanthin in Atlantic salmon, Salmo salar, fed diets with the red yeast Phaffia rhodozyma in comparison with synthetic formulated astaxanthin. Aquaculture 269:476–489. Cannon, J. E., J. B. Morgan, G. R. Schmidt, J.D. Tatum, J. N. Sofos, G. C. Smith, R. J. Delmore, and S. N. Williams. 1996. Growth and fresh meat quality characteristics of pigs supplemented with vitamin E. J. Anim. Sci. 74:98–105. Carr, C. C., D. D. Johnson, J. H. Brendemuhl, and J. M. Gonzalez. 2010. Fresh pork quality and shelf-life characteristics of meat from pigs supplemented with natural astaxanthin in the diet. Prof. Anim. Sci. 26:18–25. Chien, Y. H., and S. C. Jeng. 1992. Pigmentation of kuruma prawn, Penaeus japonicus Bate, by various pigment sources and levels and feeding regimes. Aquaculture 102:333–346. Chew, B. P., B. D. Mathison, M. G. Hayek, S. Massimino, G. A. Reinhart, and J. S. Park. 2011. Dietary astaxanthin enhances immune response in dogs. Vet. Immunol. Immunopathol. 140:199–206.
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References
This article cites 32 articles, 4 of which you can access for free at: http://www.journalofanimalscience.org/content/92/1/171#BIBL
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