J. Appl. Poult. Res.
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J APPL POULT RES 2008. 17:498-504. doi:10.3382/japr.2008-00058
© 2008 Poultry Science Association
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Research Reports

Skin Pigmentation Evaluation in Broilers Fed Different Levels of Natural Okra and Synthetic Pigments

G.-D. Liu*,1, G.-Y. Hou*, D.-J. Wang*, S.-J. Lv{dagger},1, X.-Y. Zhang*, W.-P. Sun* and Y. Yang{dagger}

* Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences, 571737, Danzhou, Hainan, China {dagger} College of Agriculture and Forestry Science, Linyi Normal University, 276000, Linyi, Shandong, China

1 Corresponding authors: liuguodao{at}126.com and lvshenjin_yang{at}sina.com


   SUMMARY
TOP
 SUMMARY
DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Broiler carcass skin color is important in China, the United States, Mexico, and other countries. The present study evaluated the use of natural and synthetic pigments in broiler diets at different commercial levels. The experiment included 288 fifty-day-old Da-Ma-Hua birds, divided into 6 treatments. Birds in 4 treatments were fed a basal diet consisting of 2, 3, 4, or 5% okra [Abelmoschus esculentus (L.) Moench Meth., also known as abelmosk or ram-horn bean] meal, respectively. Birds in another treatment received a basal diet without okra, and birds in a sixth treatment were fed a blend of 25 g/metric ton of 10% canthaxanthin and 50 g/metric ton of 10% carotenoic acid, β-apo-8'-ethylesters. Each treatment consisted of 3 replicates of 16 birds each. The experiment lasted 6 wk. Skin color was measured with a Kemin color fan after slaughter and chilling at wk 2, 3, 4, 5, and 6 of treatment. Pigmentation of the chicken skin and abdominal fat were significantly improved (P < 0.05) in the 4 and 5% okra treatments. The pigmentation effect reached a satisfactory level after 4 wk of treatment. The rank of pigmentation in different parts of the body of a bird was shank > breast > abdomen > back. The addition of okra meal had no significant influence on daily gain or the feed-to-gain ratio (P > 0.05). This study shows that xanthophyll-rich okra meal can be used as a natural pigment source in poultry feed, which may allow pigment use and feed costs to be reduced.

Key Words: poultry pigmentation • okra • xanthophyll • Da-Ma-Hua • color evaluation


   DESCRIPTION OF PROBLEM
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Pigmentation is an important factor in consumer acceptance and in the perceived quality of broilers in many countries [1, 2]. Pigments have been applied for nearly 40 yr in China, and their use has been approved worldwide. Pigments are a kind of additive that can increase the color of broilers and aquaculture animal products. They cannot be synthesized in animal bodies but can be transformed and metabolized, so they must be ingested from feed [3]. Many studies have indicated that the primary compounds with a coloring role in poultry products are carotenoids, namely, xanthophyll, the concentrated extracts from marigold meal (natural xanthophyll), capsanthin, and canthaxanthin [4–7].

Several natural sources of pigments are used in poultry feed, mainly yellow corn, corn gluten meal, and dehydrated alfalfa meal [1]. In China, the use of pigments has gradually changed from synthetic colorants to natural ones [8]. Some leaf powders or extracts from plants can be used directly to pigment broiler skin and egg yolks, producing a more desirable pigmentation as well as health benefits to the animals [8, 9]. In recent years, the use of natural colorants has been actively exploited in China and other countries, with xanthophylls and carotenoids of plant origin becoming the main sources of natural feed colorants because of their many advantages, such as safety, nontoxicity, strong biological activity, and greater bioavailability. Xanthophyll was found to produce better pigmentation in egg yolks and chicken skin when its content reached 60 mg/kg in the feed [10]. Another study stated that feeding a diet with 8 to 12% alfalfa meal (containing 500 mg/kg of carotenoids) caused the egg yolks and skin color of the birds to deepen [11]. In production, lutein (12 to 25 mg/kg) from yellow corn in feed constitutes the basis of egg yolk color. Generally, raw materials containing lutein pigment can be added to animal feed to obtain a deeper yolk color. Synthetic pigments have the disadvantage of being more expensive and lacking safety [8, 10]. In contrast, the natural colorant products are inexpensive, are of high quality, and may be beneficial for human health.

Among the natural products, marigold meals and concentrates have been the most widely accepted for commercial use in poultry feeds. However, few papers have dealt with okra powder pigments. Okra [Abelmoschus esculentus (L.) Moench Meth., also known as abelmosk or ram-horn bean], is a hairy annual or biennial plant having flowers with crimson centers that is native to tropical Asia. It is cultivated for its seed and the healthful vegetables it produces [12]. Okra, which is planted in the northern and southern areas of China as well as other areas of the world, is a vegetable that is tolerant of long hours of direct sunlight; is naturally fond of warmth; is heat, drought, and moisture resistant; and has broad adaptability to soils. This plant can be grown twice per year throughout the tropical and subtropical regions. Research on the cultivation and utilization of okra has mainly focused on several aspects, including its cultivation as a vegetable, as a medicine and for health care, as a beverage, and in gardening. The vegetable it produces contains many nutritious ingredients: 100 g of dry, tender okra pods includes 2.11 g of deoxidized sugar, 1.06 g of cellulose, 2.44 g of CP, 0.682 g of carotene, 26.5 mg of vitamin C, 1.25 mg of vitamin A, 10.2 mg of vitamin B, and many minerals, having slightly more than common vegetables and fruits [13]. The okra stem and leaf contain 17.47% CP, 13.48% crude ash, 10.9% crude fiber, 7.08% crude fat, and 51.07% nitrogen-free extract [12, 13]. Stems and leaves were used to formulate the diets in this study. The objective of this study was to evaluate the efficiency of okra as a natural pigment source when supplemented at different levels based on a standard (corn-wheat-soybean) diet.


   MATERIALS AND METHODS
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
For the trial, 500 Da-Ma-Hua broiler chicks [14] from the same brood were maintained on soil covered with a mat in open houses, with feed and water supplied ad libitum from 1 to 50 d of age. A total of 288 broilers with nearly the same shank skin color and BW (average 50-d BW: 633 ± 8 g) were then selected and transferred to 3-tier battery brooding cages equipped with nipple autodrinkers. All chicks were wing-banded for individual identification. These broilers were distributed to 6 different dietary treatments at random, with 3 replicates of 16 broilers each, 4 pens/replicate, with 4 birds per pen (a total of 72 pens). The 6 experimental diets consisted of OM-2, the basal diet plus 2% okra meal [15]; OM-3, the basal diet plus 3% okra meal; OM-4, the basal diet plus 4% okra meal; OM-5, the basal diet plus 5% okra meal; OM-0, the basal diet without okra meal; and SP, the basal diet plus a combination of 25 g/metric ton of Carophyll Red and 50 g/metric ton of Carophyll Yellow (chemically synthesized colorants containing 10% canthaxanthin and 10% carotenoic acid, β-apo-8'-ethylesters), respectively [16]. The experiment was conducted from July 18 to August 30, 2007, at the livestock center of the Tropical Crops Genetic Resources Institute, which is affiliated with the Chinese Academy of Tropical Agricultural Sciences. All the experimental chickens were fed pelleted, mixed feed produced by the integrated feed-processing plant at the Chinese Academy of Tropical Agricultural Sciences (Table lGo). Disease prevention was practiced according to the vaccination schedules of the breeder farm; the health status of birds was monitored every day, and diseased birds were eliminated immediately.


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  		Table 1. Composition of the experimental diets1
 
Visual observation was done by a color-graduated visual aid color fan [17], the Kemin color fan (KCF), with minimum and maximum values ranging from 1 to 15. The KCF was used to measure pigmentation of the shank, breast, vent, back skin, and abdominal fat in wk 2, 3, 4, 5, and 6 of treatment. Two chickens per replicate were sent at random to the slaughterhouse, and 24 h after chilling the carcasses, 6 chickens/ treatment per week were evaluated. The colorimeteric values for each part of the body tested were assigned by 3 individuals. The values were averaged to obtain the mean colorimetric values for the 6 treatments. Feed intakes were recorded daily, and all birds were weighed before and after the experiment (slaughtered birds were weighed at the time of slaughter). All results were expressed as means ± SD. The values determined each week by KCF scores were tested by a paired-samples t-test. Significance was set at P = 0.05, and all analyses were performed with SPSS software [18].


   RESULTS AND DISCUSSION
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Effect of Okra Meal on Pigmentation
After 2 wk of feeding the experimental diets, pigmentation effects were not obvious in the skin of the shank, vent, breast, or back, or in the abdominal fat (Table 2Go). There were no significant differences among treatments (P > 0.05).


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  		Table 2. Pigmentation of Da-Ma-Hua chickens fed experimental or control diets for 6 wk, from 50 to 92 d of age
 
After 3 wk on the feeding trial, shank pigment of birds in experimental treatments OM-3, OM-4, and OM-5 achieved KCF scores of approximately 5.0, which differed significantly from the shank pigment scores of birds in treatment OM-2 and the comparison treatments OM-0 and SP (P < 0.05; Table 2Go); the pigmentation in other areas was not significantly different among treatments (P > 0.05). The skin presented a little deeper yellow color than in the previous period.

After 4 wk of feeding, shank skin of birds in treatments OM-2 and OM-3 showed no difference in pigmentation (P > 0.05), but pigmentation was less than that of birds in treatments OM-4 and OM-5 (P < 0.05). The skin of the vent and breast showed an obviously deeper color (KCF values were all greater than 3.0). The back skin reached a score of 3.0 only in birds in treatment OM-5, with the other scores remaining lower than 3.0. The abdominal fat reached scores of greater than 3.0 for birds in treatments OM-4 and OM-5, and these differed significantly from the scores of other treatments (P < 0.05).

After 5 wk of feeding, birds in treatment OM-5 had a shank skin KCF value of 6.0. The vent and breast skin KCF values were between 3.1 and 4.8, with the greatest scores for birds in treatment OM-5. Back skin KCF scores were greater than 3.0 for birds in treatments OM-4 and OM-5. The skin pigment of birds in treatments OM-3, OM-4, and OM-5 was significantly different from that of birds in treatments OM-0 and SP.

After 6 wk, shank skin scores were 6.3, 6.8, and 7.0 for birds in treatments OM-3, OM-4, and OM-5, respectively, which was significantly greater than the scores for birds in treatments OM-0 and SP (P < 0.05). Pigmentation of the vent and breast skin reached KCF scores of 3.2 to 5.0 in the experimental groups, whereas pigmentation of the back skin reached scores of greater than 3.0 for birds in treatments OM-3, OM-4, and OM-5. Birds in treatments OM-4 and OM-5 achieved scores greater than 5.2 in pigmentation of abdominal fat, with those in treatment OM-5 being significantly greater than in all other treatments (P < 0.05).

The average KCF value of the shank skin was approximately 3.0 for 50-d-old Da-Ma-Hua chickens. Treatments OM-3, OM-4, and OM-5 presented better pigmentation and were different from the other treatments (P < 0.05) at different testing times. The chicken shank skin showed relatively quicker pigmentation than other parts of the body of the bird. Pigmentation of the vent and breast skin began after 3 wk on the feeding trial, basically achieving scores greater than 3.0 and presenting an ideal yellow color. Pigmentation of the back skin was relatively slower, with birds in treatment OM-5 reaching KCF scores of 3.0 at 4 wk and birds in treatments OM-3, OM-4, and OM-5 all achieving scores greater than 3.0 by wk 6. Pigmentation of the abdominal fat reached scores of 3.0 or above only for birds in treatment OM-5 on wk 3, for birds in treatments OM-4 and OM-5 on wk 4, and for birds in treatments OM-2, OM-3, OM-4, and OM-5 on wk 6. A significant difference was found among experimental groups OM-3, OM-4, and OM-5 (P < 0.05), and these groups were significantly different from the comparison groups OM-0 and SP (P < 0.05).

Cost Analysis of Pigmentation and Daily Gain
Analysis of pigmentation cost was carried out under the situation in which the nutritional level of each dietary treatment was relatively consistent across all groups. There were no significant differences among them in daily BW gain and feed intake (P > 0.05; Table 3Go).


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  		Table 3. Daily BW gains and pigmenting cost analysis1
 
All treatment groups had feed prices nearly equivalent to those of the control group, except for the SP treatment, which had the greatest feed price. The increase in feed cost of 60.0 yuan/metric ton was due to the combination of 25 g/metric ton of Carophyll Red and 50 g/metric ton of Carophyll Yellow (Carophyll Red, 1, 200 yuan/ kg; Carophyll Yellow, 600 yuan/kg) in spite of their poorer pigmentation ability (Table 3Go). The inclusion of okra stem and leaf meal in poultry diets for pigmentation could also provide other nutrients, giving it an advantage over synthetic pigments. Therefore, in terms of the cost and coloring effect, the okra stem and leaf powder was better than Carophyll Red or Carophyll Yellow as a colorant for broiler chickens.

Skin Pigmentation Performance
It is a characteristic of chickens for xanthophylls to accumulate in the body [19]. Consequently, xanthophylls have gained economic interest for coloring broiler skin. It is well known that the intensity as well as the color (yellow-red) can be controlled by the concentration and type of dietary xanthophylls [20, 21]. In 1995, xanthophylls were authorized as a food supplement by the US Food and Drug Administration for use in foodstuffs and beverages, and they have a reputation as "plant gold" in international markets. Carotenoids have been recognized by the Food and Agriculture Organization of the United Nations as being an excellent nutritious class A pigment that can be used as a food additive or nutrition supplement, and have been approved for application in 52 countries [22]. The market is approximately 1,000 metric tons every year. Therefore, the marketing prospect of exploiting carotenoid resources is greatly anticipated for the main kinds of tropical plants. Moreover, there are large differences in carotenoid content among plants from different habitats and of different breeds. Planting experiments with marigolds indicated that the hours of exposure to light was the main factor contributing to plants from different habitats and of different cultivars having obviously different xanthophyll contents and fresh flower outputs [12]. In Hainan, because of the advantages of its abundant sunlight, absence of frost year round, and high biological output, some research studies, such as the selective breeding of new varieties of tropical plants with a high content of carotenoids and planting techniques to produce a high yield, should be conducted to ensure that the supply of raw materials can meet the growing market need for carotenoids.

Xanthophylls are the main source of pigmentation on broiler skin. Because okra has a greater content of xanthophylls, supplementation of okra meal in the grower diet could produce yellow shank skin, body surface skin, and abdominal fat in broilers. Moreover, the degree of yellowness increased remarkably with the amount of okra supplemented. In the present experiment, it took approximately 3 wk for the shank skin of the trial chickens to present an obvious yellow color; these results were in agreement with the report by Branellec [23] that zeaxanthin and canthaxantin are mainly deposited in broiler shanks. After 3 wk, shank skin KCF values of greater than 3.0 were achieved for birds in treatments OM-4 and OM-5, and after 4 wk, broilers in all experimental treatments basically had better pigmentation of the skin, especially those in the OM-4 and OM-5 treatment groups. In a previous study, the RCF values of egg yolks showed an obvious increase with the addition of extracts from paprika as a colorant in layer diets [9], a result that was quite similar to those from the okra meal feeding trials. These all found that the pigmentation of chicken skin is a process during which pigment accumulates continuously. In addition, after 6 wk of feeding, birds in the OM-0 and SP treatments had the lowest RCF values, which were clearly different from the RCF values of birds in the other treatments, indicating that the desirable skin and fat pigmentation could be achieved by natural pigments. Birds in the SP treatment had the lowest RCF values owing to their physiology and the lower absorption, metabolism, or deposition of Carophyll Red and Carophyll Yellow compared with natural pigment sources [1, 11]. In the present study, we found an enhanced bioavailability of free okra. This could also improve the bioavailability of xanthophylls and possibly enhance the efficiency of xanthophyll deposition in the skin of the birds [24]. Some researchers have reported that the more lipophilic lutein esters are utilized better than crystalline lutein [25], and they have found comparable concentrations of lutein in the chicken plasma regardless of whether free or esterified xanthophylls were fed [26]. Thus, there is an ongoing discussion on the ideal form with the greatest bioavailability [26, 27].


   CONCLUSIONS AND APPLICATIONS
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
REFERENCES AND NOTES
 

  1. Okra meal can be used successfully to provide pigment in broiler diets.
  2. The degree of pigmentation in different parts of the chicken body was in the order shank > breast > abdomen > back.
  3. The addition of okra meal in chicken diets had no significant influence on daily gain and the feed-to-gain ratio.
  4. The results suggest definite value for the exploitation and use of carotenoid resources in tropical plants.


   ACKNOWLEDGMENTS
 
We thank Gao-Shan (Beijing Normal University, Beijing, China) and Anna M. Pérez-Vendrell (IRTA, Constanti, Tarragona, Spain) for their helpful comments and suggestions. This research was supported by the Hainan Natural Science Foundation (No. 30508).


   REFERENCES AND NOTES
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 

  1. Castañeda, M. P., E. M. Hirschler, and A. R. Sams. 2005. Skin pigmentation evaluation in broilers fed natural and synthetic pigments. Poult. Sci. 84:143–147.[Abstract/Free Full Text]
  2. Ouart, M. D., D. E. Bell, D. M. Janky, M. G. Dukes, and J. E. Marion. 1988. Influence of source and physical form of xanthophylls pigment on broiler pigmentation and performance. Poult. Sci. 67:544–548.[Web of Science][Medline]
  3. Breithaupt, D. E. 2007. Modern application of xanthophylls in animal feeding—A review. Trends Food Sci. Technol. 18:501–506.[CrossRef]
  4. Marusich, W. L., and J. C. Bauernfeind. 1981. Oxycarotenoids in poultry feeds. Pages 320–441 in Carotenoids as Colorants and Vitamin A Precursors. Academic Press, New York, NY.
  5. Pérez-Vendrell, A. M., J. M. Hernádez, L. Llauradó, J. Schierle, and J. Brufau. 2001. Influence of source and ratio of xanthophyll pigments on broiler chicken pigmentation and performance. Poult. Sci. 80:320–326.[Abstract/Free Full Text]
  6. Fletcher, D. L., C. M. Papa, and F. X. Tirado. 1986. The effect of saponification on the broiler coloring capability of marigold extracts. Poult. Sci. 65:1708–1714.[Web of Science]
  7. Blanch, A., and J. M. Hernández. 2000. Red carotenoids for optimal yolk pigmentation. Feed Mix. 8:9–12.
  8. Zhou, L. J., J. Chen, Y. X. Li, and G. Z. Li. 2003. Skin pigmentation evaluation in broilers with natural xanthophyl. Feed Ind. 24:36–40.
  9. Lu, Y. P., H. F. Zhang, J. Fu, and F. Z. Liu. 2005. Effect of paprika extract supplement on egg yolk color of layer fed wheat-based diets. J. Anim. Nutr. 17:28–32.
  10. Li, D. F. 2003. The Feed Cyclopedia in China. China Agriculture Press, Beijing, China.
  11. Xie, Z. Q., and S. Q. Niu. 2004. The Production Technology and Quality Standard of Natural Plant Additives. China Agricultural Science and Technical Press, Beijing, China.
  12. Feng, G. M., and X. H. Xu. 1984. Flora of China. Vol. 49. China Scientific Press, Beijing, China.
  13. Liu, G.-D., D.-J. Wang, G.-Y. Hou, and Y.-F. Chen. 2007. Effective of pigmentation in chicken vitelline with powdery Abelmoschus esculentus additive. Chin. Agric. Sci. Bull. (in press)
  14. Da-Ma-Hua birds: a poultry breed native to Hainan Province, China. The typical slaughter age and BW are 13 to 14 wk and 1,700 to 1,900 g, respectively.
  15. The natural pigments of okra meal (powder) were provided by the Tropical Crops Genetic Resources Institute, Danzhou, Hainan, China.
  16. Carophyll Red and Carophyll Yellow: Roche Inc., Shanghai, China.
  17. Kemin color fan: Kemin Industries, Des Moines, IA.
  18. SPSS. 2003. User’s Guide, Version 11.0. SPPS Inc., Chicago, IL.
  19. Hencken, H. 1992. Chemical and physiological behavior of feed carotenoids and their effects on pigmentation. Poult. Sci. 71:711–717.[Web of Science][Medline]
  20. Chen, B. H., and S. H. Yang. 1992. An improved analytical method for the determination of carotenes and xanthophylls in dried plant materials and mixed feeds. Food Chem. 44:61–66.[CrossRef]
  21. Lai, S. M., J. I. Gray, and C. J. Flegal. 1996. Deposition of carotenoids in eggs from hens fed diets containing saponified and unsaponified oleoresin paprika. J. Sci. Food Agric. 72:166–170.[CrossRef][Web of Science]
  22. Zhu, H. X., and J. X. Zheng. 2005. Xanthophyl structure, distribution, transformation nature and physiological function. China Food Addit. 5:48–55.
  23. Branellec, J. C. 1985. La pigmentation du poulet de chair. Aliscope 85:1–13.
  24. Hamilton, P. B., F. I. Tirado, and F. Garcia-Hernandez. 1990. Deposition in egg yolks of the carotenoids from saponified and unsaponified oleoresin of red pepper (Capsicum annuum) fed to laying hens. Poult. Sci. 69:462–470.[Web of Science]
  25. Philip, T., C. W. Weber, and J. W. Berry. 1976. Utilization of lutein and lutein-fatty acid esters by laying hens. J. Food Sci. 41:23–25.[CrossRef][Web of Science]
  26. Breithaupt, D. E., P. Weller, and M. A. Grashorn. 2003. Quantification of carotenoids in chicken plasma after feeding free or esterified lutein and capsanthin using high-performance liquid chromatography and liquid chromatography-mass spectrometry analysis. Poult. Sci. 82:395–401.[Abstract/Free Full Text]
  27. Bowen, P. E., S. M. Herbst-Espinosa, E. A. Hussain, and M. Stacewicz-Sapuntzakis. 2002. Esterification does not impair lutein bioavailability in humans. J. Nutr. 132:3668–3673.[Abstract/Free Full Text]




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