Meat Color Modification in Broiler Chickens by Feeding Yeast Phaffia rhodozyma Containing High Concentrations of Astaxanthin

2001 Poultry Science Association, Inc.

MEAT COLOR MODIFICATION IN BROILER CHICKENS BY FEEDING YEAST PHAFFIA RHODOZYMA CONTAINING HIGH CONCENTRATIONS OF ASTAXANTHIN

K. MATSUSHITA and H. KOMIYAMA Yamanashi Prefecture Livestock Experimental Station, Tamaho-machi 409-3812, Japan H. TSUNEKAWA and H. NAGAO Mercian Corporation, Tokyo 104-8305, Japan

Primary Audience: Nutritionists, Poultry Producers, Feed Manufacturers, Researchers

SUMMARY Three experiments were conducted to evaluate the potential of Phaffia rhodozyma, a yeast containing high levels of astaxanthin (Ax), with or without cell-wall fracturing, to modify meat color in broiler chickens. Experimental diets supplemented with non-treated Phaffia yeast or cellwall fractured yeast to provide up to 15, 20, and 30 ppm Ax were fed to 4- or 5-wk-old chickens for 14 or 21 d. Diets supplemented with Phaffia yeast did not influence performance of broilers or edible meat yields. Concerning color analysis of edible meats, for abdominal adipose tissues and breast skin using Minolta reflectance colorimetry, the lightness (L* value) and yellowness (b* value) of the tissues were not meaningfully influenced by the yeast-supplemented diets. However, the redness (a* value) of all tissues measured was significantly increased by the yeast-supplemented diet. The effect was heightened by supplementing fractured yeasts in the broiler feed in proportion to dietary Ax concentration; Ax was detected in edible meats and liver in the concentration range from 0.1 to 1.1 µg/g tissue, and the concentration was mostly dependent on the dietary Ax concentration. These results show that the cell-wall fractured Phaffia yeast containing high concentrations of Ax can be a useful source of Ax for the modification of meat color, thus meeting consumer preferences in relation to the qualities of poultry meat.

Key words: Astaxanthin, broiler chickens, meat color, meat yield, yeast 2001 J. Appl. Poult. Res. 10:154–161

1

To whom correspondence should be addressed.

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Y. AKIBA1, K. SATO, and K. TAKAHASHI Laboratory of Animal Nutrition, Graduate School of Agricultural Science, Tohoku University, Sendai-shi 981-8555, Japan Phone: +81 (0) 22-717-8688 FAX: +81 (0) 22-717-8691 e-mail: [email protected]

AKIBA ET AL.: MEAT COLOR MODIFICATION

DESCRIPTION OF PROBLEM

studies examining the pigmentation of meats and the tissue carotenoid concentrations in broiler chickens fed diets with graded levels of Phaffia yeast with or without cell-wall fracturing.

MATERIALS AND METHODS BIRDS AND DIETS Broiler chicks were obtained from a commercial hatchery at 1 d of age. They were housed in electrically heated batteries in Experiment 1 and on the floor in Experiments 2 and 3 and were provided with water and a commercial starter diet (0 to 3 wk of age) and a finisher diet (after 3 weeks of age) for ad libitum intake prior to commencing each experimental treatment. At the beginning of each experiment chicks were selected from a 1.5fold larger population to obtain uniformity of body weights among the birds. In Experiment 1, a commercial starter diet (ME, 3,150 kcal/kg; CP, 22.0%) and finisher diet (ME, 3,150 kcal/kg; CP, 18.0%), in which yellow corn was the major cereal, were used as a basal diet. For Experiments 2 and 3, a low carotenoid diet and a standard diet were provided, respectively (Table 1). Chickens had free access to experimental feed and water at all times. EXPERIMENT 1 Sixteen male broiler chickens (Ross) aged 4 wk, each weighing 1.13 ± 0.1 kg, were assigned at random to two groups of eight birds and reared in a wire-bottomed cage under conditions of controlled temperature (24 ± 1°C) and continuous light. They were fed a commercial starter diet for 14 d that was either supplemented or not with 1.21% (w/w) Phaffia yeast (non-treated). The yeast-supplemented diet provided 20 ppm Ax. EXPERIMENT 2 Three hundred thirty-six female broiler chicks (Cobb) aged 5 wk that weighed 1.70 ± 0.05 kg on average were assigned at random to two groups of 168 with three replicates of 56 birds each. The birds were reared on a solid floor in a windowless house. They were fed for 21 d on a low carotenoid diet (Table 1) with or without supplementation with 1.21% (w/w) Phaffia yeast (nontreated). The presence of the yeast provided 20 ppm Ax.

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The visual appearance of food, including color, is a major concern of consumers in the marketplace. In poultry meats, skin color was considered a major quality issue for the consumer’s final evaluation of the product during the time when most poultry meat was purchased as a whole carcass. Lipstein [1] reviewed the inclusion of several factors into meat quality, with particular reference to skin pigmentation, in broilers. Along with the recent increase in consumption of filleted meat in developed countries, the color of breast and thigh meats has attracted the attention of consumers engaged in the selection of raw meat products [2, 3]. This is, particularly in Japan, evidenced by the recent preference of consumers for branded quality meats including cross-breeds of Japanese native chickens, the meats of which are characterized by strong-colored and reddish fillets [4]. Froning [3] reviewed the many live bird production factors associated with poultry meat color. These included genetics, environmental condition of poultry housing, pre-slaughter environment, slaughter and chilling conditions, processing and storage conditions, and dietary regime. Because meat color is mostly determined by heme pigments in muscles, such as myoglobin, hemoglobin, and cytochrome c, and the myoglobin concentration in muscles is considered to be exclusively due to genetic factors [3, 5, 6], the dietary manipulation of meat color has received relatively little attention apart from a few papers describing certain changes in meat color caused by fasting [7] and supplementation of nitrite [8]. However, the development of dietary manipulation of meat color could become a focal point of animal scientists as poultry producers attempt to attract more consumers. A red-pigmented yeast, Phaffia rhodozyma, contains high concentrations of Ax and has been used as an excellent dietary pigment source to produce pink flesh in salmonoids [9, 10]. Considering our previous papers [11, 12, 13], which showed that supplementation of Phaffia yeast (on a ppm concentration basis) to layer diets improved egg yolk color by intensifying the redness, we are interested in whether the Phaffia yeast would improve pigmentation of broiler meats. Consequently, we report here on the results of

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156 TABLE 1. Composition of experimental diets

INGREDIENT

LOW CAROTENOID DIET

a fine powder and cooled to room temperature as quickly as possible.

STANDARD DIET

(%)

Calculated analysis CP (%) ME (kcal/kg)

46.60 20.00 10.00 16.00 3.00 4.00 3.50 — — 5.30 0.10

67.30 — — 17.20 3.00 3.00 3.50 1.00 3.30 — 0.10

0.20 1.00 0.20 0.20

0.20 1.00 0.20 0.20

18.3 3.15

18.3 3.15

A

See Akiba et al. [11].

EXPERIMENT 3 Four hundred eighty female broiler chicks (Cobb) aged 5 wk that weighed 1.76 ± 0.06 kg on average were assigned at random to four groups of 120 with four replicates of 30 birds each. The birds were reared in the same way as in Experiment 2. They were fed on a standard diet (Table 1) for 21 d. One group was used as the control with no added Ax. The other three groups received either a diet with non-treated Phaffia yeast [0.6% (w/w)] to provide 15 ppm Ax or diets with cell-fractured Phaffia yeast [0.6 and 1.2% (w/w)] to provide 15 and 30 ppm Ax, respectively. PHAFFIA YEAST The yeast, Phaffia rhodozyma, fermented in a jar, was freeze-dried at room temperature. The chemical composition of the yeast has been described in a previous paper [11]. The total carotenoid and Ax concentrations of the yeast used in both Experiments 1 and 2 were 2,524 and 1,646 ppm, respectively. Those used in Experiment 3 were 3,717 and 2,435 ppm, respectively. For the preparation of cell-wall fractured yeast, Phaffia yeast was mechanically ground into

The body weights and feed consumption of chickens were recorded every week. At the end of Experiment 1, all birds were bled, and breast muscles (Pectoralis major and Pectoralis minor) and thigh muscles were dissected and weighed. In Experiments 2 and 3, all birds were bled by cutting the carotid artery. Feather removal was accomplished in a free-action picker after subscalding at approximately 60°C. Heads and shanks were removed, and the remaining carcasses were chilled for 24 h prior to removing meat and tissues. Breast meat (Pectoralis major and Pectoralis minor), thigh muscles, wings, livers, and abdominal fat pads were dissected and weighed. The percentage yield of edible meat (sum of breast and thigh meat) was calculated on the basis of carcass weight. ANALYSIS The color of each sample was determined using a Minolta reflectance colorimeter [14] and is reported according to the CIE (Commission Internationale de Enluminure) system values of L*, a*, and b*. To accomplish uniformly the determination of meat color, colorimetry was performed on a fixed portion of breast and thigh meat, abdominal fat pad, and breast skin, respectively, for each experiment. The meat samples (Pectoralis major, Pectoralis minor, and Sartorius) and liver samples were used for the extraction and determination of carotenoid and Ax concentrations. Briefly, samples were minced with 1.6 times (w/v) 0.1 M NH4 buffer and then sonicated. The homogenates were mixed with an extraction solvent of ethanol and hexane (1:1) with vigorous agitation and centrifuged at 2,500 rpm for 10 min. The precipitate was subjected to extraction by hexane. After centrifugation, the supernatant was dried in vacuo and dissolved in acetone. The Ax and carotenoid levels in aliquots were determined using HPLC [15] as previously described [11]. STATISTICAL ANALYSIS All results are expressed as means ± SD. In each experiment, an SAS application package

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Yellow corn Barley Grain sorghum Soybean meal Rapeseed meal Fish meal Meat and bone meal Corn gluten meal Yellow grease Tallow DL-Methionine Calcium phosphate, dibasic Calcium carbonate Sodium chloride Vitamin mixtureA

MEASUREMENTS

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TABLE 2. Effect of diets supplemented with Phaffia yeast for 14 d from 28 d of age (Experiment 1) and for 21 d from 35 d of age (Experiment 2) on meat color in broiler chickensA BREAST MEAT TREATMENT

Experiment 2D L* Value Control Phaffia, 20 ppm Ax a* Value Control Phaffia, 20 ppm Ax b* Value Control Phaffia, 20 ppm Ax

Pectoralis minor

45.9 ± 1.2 44.6 ± 1.4

47.7 ± 1.2 44.2 ± 2.0*

THIGH MEAT Satorius

ABDOMINAL ADIPOSE TISSUE

50.0 ± 1.6 47.5 ± 1.8

NDE ND

4.4 ± 0.9 5.7 ± 0.6*

4.0 ± 0.9 5.9 ± 0.8*

6.8 ± 1.0 8.1 ± 0.8*

ND ND

5.8 ± 2.9 5.3 ± 1.5

5.6 ± 2.9 3.6 ± 2.7

4.7 ± 3.1 6.1 ± 4.1

ND ND

47.1 ± 1.7 45.1 ± 1.1

43.4 ± 1.9 42.2 ± 2.1

41.3 ± 1.8 39.7 ± 1.7

68.2 ± 2.8 66.4 ± 1.6

2.5 ± 0.5 4.4 ± 0.9* 11.8 ± 1.1 12.4 ± 0.9

2.6 ± 0.7 4.3 ± 0.7* 10.7 ± 0.9 11.0 ± 0.9

4.1 ± 1.0 6.2 ± 0.8* 10.2 ± 0.7 10.8 ± 0.8

0.5 ± 1.5 3.1 ± 1.1* 18.3 ± 1.9 17.5 ± 1.6

A

Lightness (L*), redness (a*), and yellowness (b*) values were determined by Chroma Meter. Body weight at start of Experiment 1 was 1.13 ± 0.1 kg (mean ± SD with eight observations). C Ax = astaxanthin. D Body weight at start of Experiment 2 was 1.70 ± 0.05 kg (mean ± SD with 15 observations). E ND = not determined. *Significantly different (P < 0.05) from the control value. B

was used for statistical calculations [16]. Data in Experiments 1 and 2 were subjected to Student’s t-test analyses. Group data for multiple comparisons in Experiment 3 were analyzed by ANOVA using a general linear models procedure followed by Duncan’s multiple range test. Levels of statistical significance were based on values of P < 0.05.

RESULTS AND DISCUSSION EXPERIMENT 1 Average feed intake and body weight gain were not significantly different between the two groups (data not shown). Results of meat color evaluation are presented in Table 2. A significant increase in a* values for both breast and thigh meat and in L* value for Pectoralis minor were observed when diets containing the yeast supplement (20 ppm Ax) were fed.

EXPERIMENT 2 No significant changes in feed intake, body weight gain, edible meat yield, or yields of breast and thigh meat were observed when chickens were fed diets supplemented with non-treated Phaffia yeast (data not shown). Table 2 shows that L* and b* values of the edible muscles and adipose tissues were not modified by the yeastsupplemented diet (20 ppm Ax). On the other hand, the a* value in all muscle and adipose tissues determined was significantly increased by the yeast-supplemented diet for 21 d beginning when the chickens were 35 d of age. EXPERIMENT 3 Performance and edible meat production was not influenced by either the non-treated or cellwall fractured Phaffia yeast-supplemented diets (Table 3). The results of the color evaluation of meats, adipose tissue, and skin are presented in

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Experiment 1B L* Value Control Phaffia, 20 ppm AxC a* Value Control Phaffia, 20 ppm Ax b* Value Control Phaffia, 20 ppm Ax

Pectoralis major

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TABLE 3. Effect of diets supplemented with Phaffia yeast for 21 d from 35 d of age on performance and edible meat yield in broiler chickensA (Experiment 3)

TREATMENT

BODY WEIGHT GAIN

FEED INTAKE (kg)

BREAST MEAT Pectoralis major

Pectoralis minor

(% of carcass wt)

THIGH MEAT

(g)

3.86 ± 0.11 3.79 ± 0.22

1.39 ± 0.05 1.36 ± 0.09

43.2 ± 0.7 43.5 ± 1.1

500 ± 30 509 ± 79

111 ± 7 113 ± 3

592 ± 38 590 ± 40

3.90 ± 0.06 3.97 ± 0.07

1.37 ± 0.02 1.34 ± 0.06

43.4 ± 0.5 43.7 ± 0.6

507 ± 20 513 ± 34

114 ± 6 113 ± 5

597 ± 20 606 ± 16

Body weight at start of experiment was 1.76 ± 0.06 kg. Values for feed intake and body weight gain represent means ± SD over four observations. Values for edible meat production represent means ± SD over 20 observations. B Ax = astaxanthin. A

Table 4. No significant changes in L* and b* values of breast meats, thigh meat, abdominal adipose tissue, or breast skin were detected between treatments with the exception of a low L* value for adipose tissue in chickens fed the diet supplemented with cell-wall fractured Phaffia yeast (30 ppm Ax). Feeding the non-treated yeastsupplemented diet (15 ppm Ax) numerically increased the a* values of breast meat, thigh meat, and adipose tissue, respectively. The cell-wall

fractured yeast-supplemented diet significantly increased a* values of meat, adipose tissue, and skin; the effects tended to be more pronounced at the 30 ppm level compared with the 15 ppm level. The yeast-supplemented diets resulted in decreases of the coefficient of variance (SD/mean value) of the a* value in all meats sampled. Total carotenoid concentrations in most of the tissues sampled (Table 5) were increased by the yeast-supplemented diets, but the increase

TABLE 4. Effect of diets supplemented with Phaffia yeast for 21 d from 35 d of age on meat color in broiler chickens (Experiment 3)A BREAST MEAT TREATMENT L* Value Control Phaffia, 15 ppm AxB Phaffia (fractured) 15 ppm Ax 30 ppm Ax a* Value Control Phaffia, 15 ppm Ax Phaffia (fractured) 15 ppm Ax 30 ppm Ax b* Value Control Phaffia, 15 ppm Ax Phaffia (fractured) 15 ppm Ax 30 ppm Ax

Pectoralis major

Pectoralis minor

41.7 ± 2.1 41.5 ± 2.3 40.5 ± 1.9 39.6 ± 2.1

THIGH MEAT Satorius

ABDOMINAL ADIPOSE TISSUE

BREAST SKIN

37.8 ± 1.4 37.3 ± 2.2

42.0 ± 2.7 42.6 ± 2.8

67.0 ± 1.0a 66.9 ± 2.0a

57.1 ± 3.9 56.6 ± 4.1

36.5 ± 2.0 36.3 ± 1.8

41.2 ± 2.4 41.3 ± 2.6

65.6 ± 2.4ab 64.8 ± 1.4b

56.1 ± 4.5 56.7 ± 3.3

−0.4 ± 1.4b 0.1 ± 0.5b

0.2 ± 0.8b 0.5 ± 0.5b

8.4 ± 1.3b 8.9 ± 1.4b

−1.2 ± 1.8b −0.8 ± 1.0b

−2.3 ± 1.6b −1.9 ± 1.1b

1.5 ± 0.7a 2.4 ± 1.0a

1.2 ± 0.7a 1.9 ± 0.8a

10.9 ± 1.6a 10.3 ± 1.4a

1.8 ± 1.3a 3.8 ± 1.5a

−0.3 ± 1.9a −0.1 ± 1.2a

8.5 ± 1.5 8.2 ± 1.2

7.4 ± 0.9 7.5 ± 1.1

11.9 ± 1.4 12.2 ± 1.1

15.8 ± 2.0 15.8 ± 2.1

8.8 ± 2.1 8.4 ± 2.9

8.8 ± 0.6 8.6 ± 0.9

7.6 ± 0.8 7.7 ± 0.9

13.0 ± 1.2 12.7 ± 1.3

15.9 ± 1.8 16.0 ± 1.7

10.2 ± 3.4 8.3 ± 2.5

Means with different superscripts in a column are significantly different (P < 0.05). Lightness (*L), redness (a*), and yellowness (*b) values were determined by Chroma Meter (mean ± SD over 20 observations). B Ax = astaxanthin. a,b A

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Control Phaffia, 15 ppm AxB Phaffia (fractured) 15 ppm Ax 30 ppm Ax

EDIBLE MEAT YIELD

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MEAT COLOR CHANGES BY FEEDING PHAFFIA YEAST The present data show that the a* value of edible meats in broiler chickens is intensified by feed supplemented with Phaffia yeast, which contains a high concentration of Ax. This effect is emphasized for breast meat compared with thigh meat. The intensified redness is easily visible as illustrated in Figure 1. To date, dietary manipulation of meat color in broiler chickens prior to slaughter has not been thoroughly investigated; only Froning et al. [8] has reported that the inclusion of nitrite in the diet increased the redness of broiler breast meat. Hence, our results are the first to show that meat color, in particular the redness of both breast and thigh portions, can be manipulated in broiler chickens by supplementing a natural feed ingredient in the diet. Phaffia yeast with Ax is commonly used to produce pink flesh in fish [10], and we have proposed that the yeast is useful as a potent source

DEPOSITION OF AX IN MUSCLES AND LIVER Trans-Ax was detected in muscles (0.1 to 0.3 µg/g) and liver (0.3 to 1.1 µg/g) in chickens fed yeast but not in control chickens; the concentration of trans-Ax rose partly in proportion to the dietary Ax concentrations. The a* value of the breast meat was intensified with the increase of dietary Ax, although this result was not statistically significant. While Ax is partly metabolized to idoxanthin and crustaxanthin in chicken liver [20], it is likely that the pigmentation of edible meats is mainly due the Ax, which is directly

TABLE 5. Effect of diets supplemented with Phaffia yeast for 21 d from 35 d of age on carotenoids and astaxanthin (Ax) concentration of edible meats and liver in broiler chickensA (Experiment 3) TREATMENT EDIBLE MEAT AND LIVER Total carotenoids (µg/g) Pectoralis major Pectoralis minor Satorius Liver Trans-A (µg/g) Pectoralis major Pectoralis minor Satorius Liver

Control 0.84 0.90 0.73 5.98

± ± ± ± 0 0 0 0

0.07b 0.35a 0.23b 2.64c

Phaffia 15 ppm Ax

A

15 ppm Ax

30 ppm Ax

1.03 0.78 1.07 7.24

± ± ± ±

0.20a 0.14a 0.13a 2.67bc

1.12 1.09 1.27 9.77

± ± ± ±

0.24a 0.33a 0.26a 2.80b

1.05 1.19 1.42 14.30

± ± ± ±

0.27a 0.33a 0.51a 5.60a

0.10 0.03 0.10 0.36

± ± ± ±

0.06a 0.01b 0.08a 0.15b

0.17 0.14 0.12 0.85

± ± ± ±

0.12a 0.06ab 0.04a 0.44a

0.20 0.21 0.29 1.14

± ± ± ±

0.13a 0.10a 0.26a 0.48a

Means with different superscripts in a row are significantly different (P < 0.05). Means ± SD over 10 observations.

a,b,c

Phaffia (fractured)

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for pigmentation of egg yolk in laying hens [11, 12, 13]. Dietary carotenoid sources, in which the major carotenoids are lutein, zeaxanthin, cryptaxanthin, and capsanthin as well as canthaxanthin, a stabilized synthetic carotenoid, have been used to pigment egg yolk [17, 18]. Janky and Harms [19] noted that supplementation of broiler diets with canthaxanthin (4 ppm) improved shank skin color. The present data show that, in addition to altering the egg yolk color of laying hens [11, 12, 13], Ax is a potent carotenoid that can be used to pigment both the meat (muscles) and skin of broiler chickens. The redness of meat, fat, and skin was intensified by using the cell-wall fractured form of the yeast in the feed. This result is in accordance with our previous findings [13] in laying hens, in which the fractured yeast fed to hens was 3-fold as efficient as the non-treated yeast for the pigmentation of egg yolk.

was not essentially dependent on the dietary Ax level in groups given the cell-wall fractured yeastsupplemented diet. Trans-Ax was detected in all tissues sampled from chickens fed yeast-supplemented diets; concentrations ranged from 0.03 to 0.3 µg/g for muscle tissue and 0.4 to 1.1 for µg/ g of liver. The trans-Ax concentration increased numerically when diets supplemented with fractured yeast were fed in comparison with the concentration when non-treated yeast was fed and in proportion to the dietary Ax concentrations.

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incorporated into the meat. The biological function of carotenoids has received significant attention in recent years [21], and Ax shows the most prominent antioxidant activity and immuno-modulating properties in animal tissues [22, 23]. The Ax deposited (0.1 to 1.1 g/g) in tissues might be of interest in terms of preventing tissue peroxidation in chicken flesh and, thereby, might be a source of food for human consumption, which also has an additional biological function. AVAILABILITY OF PHAFFIA YEAST FOR MEAT COLOR MODIFICATION Poultry meat color is a critical quality attribute, even though the preference of consumers for meat color is variable. Current standards related to meat color in the broiler industry highlight the prevalence of somewhat pale meat, probably

because of early marketing age, in addition to the fact that color of the meat varies considerably. Dark discoloration and pale fillets are considered defects in many areas of the world [2, 3, 24]. Meats with discoloration have been reported to accompany both changes in L* and a* values [2, 24]. Because the feeding of Phaffia yeastsupplemented diets intensified the redness of breast and thigh meats with no changes in the L* values and simultaneously lessened the coefficient of variance of the a* value in all sampled meats, the yeast may be used for the manipulation of chicken meat color with no influence on the lightness (taking consumers’ preferences into consideration). Our findings that performance and edible meat yields were not influenced by the yeast-supplemented diets may encourage the practical application of Phaffia yeast in broiler feed formulation.

CONCLUSIONS AND APPLICATIONS 1. The a* value (on Minolta reflactance colorimeter) of edible meats (breast fillets and thigh fillets) was significantly increased by feeding the cell-wall fractured Phaffia yeast-supplemented diet for 3 wk, which provided 15 to 30 ppm Ax in the diets. 2. Performance and edible meat yield were not influenced by feeding the Phaffia yeast-supplemented diet for 3 wk prior to slaughter.

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FIGURE 1. Photographs of breast fillets (Pectoralis major) in broiler chickens fed cell-wall fractured Phaffia yeastsupplemented diets to provide 30 ppm astaxanthin (Ax) for 21 days from 35 days of age (Experiment 2).

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3. Astaxanthin, an antioxidant carotenoid, was deposited in the edible meat in the concentration range from 0.1 to 0.3 µg/g. 4. Phaffia yeast is practically useful as a potent source for manipulation of chicken meat color.

REFERENCES AND NOTES 2. Fletcher, D.L., 1999. Broiler breast meat color variation, pH, and texture. Poult. Sci. 78:1323–1327. 3. Froning, G.W., 1995. Color of poultry meat. Poult. Avian Biol. Rev. 6:83–93. 4. Komai, T., 1997. Branded quality chicken booms in Japan. Poult. Int. 36(3):34–35. 5. Fleming, B.K., G.W. Froning, and T.S. Yang, 1991. Heme pigment levels in chicken broilers chilled in ice slush and air. Poult. Sci. 70:2197–2200. 6. Froning, G.W., J. Daddario, and T.E. Hartung, 1968. Color and myoglobin concentration in turkey meat as affected by age, sex and strain. Poult. Sci. 47:1827–1835. 7. Lawrie, R.A., 1991. Pages 82–89 in: Meat Science. 5th ed. Pergamon Press, Oxford, England. 8. Froning, G.W., J. Daddario, T.E. Hartung, T.W. Sullivan, and R.M. Hill, 1969. Color of poultry meat as influenced by dietary nitrates and nitrites. Poult. Sci. 48:668–673.

ity of cell wall-fractured yeast, Phaffia rhodozyma, containing high concentration of astaxanthin for egg yolk pigmentation. Anim. Sci. J. 71:255–260. 14. Minolta Chroma Meter CR-200b, Minolta Camera Corp., Osaka, Japan. 15. SPD-&AV, Shimazu, Kyoto, Japan. 16. Statistical Analysis System, 1982. SAS User’s Guide: Statistics. SAS Inst., Inc., Cary, NC. 17. Belyavin, C.G. and A.G. Marangos, 1987. Natural products for egg yolk pigmentation. Pages 47–68 In: Recent Advances in Animal Nutrition. W. Haresign and D.J.A. Cole, Ed. Butterworths, London, England. 18. Karunajeewa, H., J.H. Hughes, M.W. McDonald, and F.S. Shenstone, 1984. A review of factors influencing pigmentation of egg yolks. World’s Poult. Sci. J. 40:52–65. 19. Janky, D.M. and R.H. Harms, 1983. Influence of canthaxanthin supplementation on broiler pigmentation in open and windowless houses. Poult. Sci. 62:2192–2194. 20. Schiedt, K., F.J. Leuenberger, M. Vecci, and E, Glinz, 1985. Absorption, retention and metabolic transformations of carotenoids in rainbow trout, salmon and chicken. Pure Appl. Chem. 57:685–692.

9. Andrewes, A.G., H.J. Phaff, an M.P. Starr, 1976. Carotenoids of Phaffia rhodozyma, a red-pigmented fermentation yeast. Phytochemistry 15:1003–1007.

21. Miki, W., 1991. Biological functions and activities of animal carotenoids. Pure Appl. Chem. 63:141–146.

10. Johnson, E.A., D.E. Conklin, and M.J. Lewis, 1977. The yeast Phaffia rhodozyma as a dietary pigment source for salmonoids and crustaceans. J. Fish Res. Board, Canada 34:2417–2421.

22. Jyonouchi, H., S. Sun, Y. Tomita, and M.D. Gross, 1995. Astaxanthin, a carotenoid without vitamin A activity, augments antibody responses in cultures including T-helper cell clones and suboptimal doses of antigen. J. Nutr. 125:2483–2492.

11. Akiba, Y., K. Sato, K. Takahashi, Y. Takahashi, A. Furuki, S. Konashi, H. Nishida, H. Tsunekawa, Y. Hayasaka, and H. Nagao, 2000. Pigmentation of egg yolk with yeast Phaffia rhodozyma containing high concentration of astaxanthin in laying hens fed on a low-carotenoid diet. Jpn. Poult. Sci. 37:77–85.

23. Palozza, P. and N.I. Krinsky, 1992. Astaxanthin and canthaxanthin are potent antioxidants in a membrane model. Arch. Biochem. Biophys. 297:291–295. 24. Boulianne, M. and A.J. King, 1998. Meat color and biochemical characteristics of unacceptable dark-colored broiler chicken carcasses. J. Food Sci. 63:759–762.

12. 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.

ACKNOWLEDGMENT

13. Akiba, Y., K. Sato, K. Takahashi, M. Toyomizu, Y. Takahashi, H. Tsunekawa, Y. Hayasaka, and H. Nagao, 2000. Availabil-

The authors thank Yoko Takahashi for excellent technical assistance.

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1. Lipstein, B., 1989. Meat quality in broilers, with particular reference to pigmentation. Pages 17–41 In: Recent Advance in Animal Nutrition. W. Haresign and J.A. Cole, Ed. Butterworths. London, England.