The protein oxidation of soybean meal induced by heating decreases its protein digestion in vitro and impairs growth performance and digestive function in broilers

British Poultry Science

Volumn 58, Issue 6, 2017, Pages 704-711

  Lu, P ^a   Zhang, X L ^a   Xue, W Y ^a   Wu, D W ^a   Ding, L R ^a   Wen, C ^a   Zhou, Y M ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

broiler; Digestibility; heating; protein oxidation; soybean meal

Indexed keywords

ANALYSIS; ANIMAL; ANIMAL FOOD; CHEMISTRY; CHICKEN; DIET; DIGESTION; FEMALE; GROWTH, DEVELOPMENT AND AGING; HEATING; MALE; OXIDATION REDUCTION REACTION; PHYSIOLOGY; PROTEIN DEGRADATION; PROTEIN INTAKE; RANDOMIZATION; SOYBEAN; VETERINARY;

ANIMAL FEED; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; CHICKENS; DIET; DIETARY PROTEINS; DIGESTION; FEMALE; HEATING; MALE; OXIDATION-REDUCTION; PROTEOLYSIS; RANDOM ALLOCATION; SOYBEANS;

EID: 85029439674     PISSN: 00071668     EISSN: 14661799     Source Type: Journal    
DOI: 10.1080/00071668.2017.1370535     Document Type: Article

References (58)

1. American Oil Chemists Society. 1998. Official Methods and Recommended Practices of the American Oil Chemists’ Society. 5th ed. Champaign, IL,: AOCS.
2. Anderson, M. M., J. R., Requena, J. R., Crowley, S. R., Thorpe, and J. W., Heinecke. 1999. “The Myeloperoxidase System of Human Phagocytes Generates Nε-(Carboxymethyl)Lysine on Proteins: A Mechanism for Producing Advanced Glycation End Products at Sites of Inflammation.” Journal of Clinical Investigation 104: 103–113. doi:10.1172/JCI3042.
3. Araba, M., and N. M., Dale. 1990. “Evaluation of Protein Solubility as an Indicator of Underprocessing of Soybean Meal.” Poultry Science 69: 76–83. doi:10.3382/ps.0690076.
4. Associationof Official Analytical Chemists. 1990. Official Methods of Analysis. 15th ed. Arlington, VA,: AOAC.
5. Berlett, B. S., and E. R., Stadtman. 1997. “Protein Oxidation in Aging, Disease, and Oxidative Stress.” Journal of Biological Chemistry 272: 20313–20316. doi:10.1074/jbc.272.33.20313.
6. Beveridge, T., S. J., Toma, and S., Nakai. 1974. “Determination of SH and SS-groups in Some Food Proteins Using Ellman’s Reagent.” Journal of Food Science 39: 49–51. doi:10.1111/jfds.1974.39.issue-1.
7. Boatright, W. L., and N. S., Hettiarachchy. 1995. “Spray-Dried Soy Protein Isolate Solubility, Gelling Characteristics, and Extractable Protein as Affected by Antioxidants.” Journal of Food Science 60: 806–809. doi:10.1111/jfds.1995.60.issue-4.
8. Boisen, S., and J. A., Fernández. 1995. “Prediction of the Apparent Ileal Digestibility of Protein and Amino Acids in Feedstuffs and Feed Mixtures for Pigs by in Vitro Analyses.” Animal Feed Science and Technology 51: 29–43. doi:10.1016/0377-8401(94)00686-4.
9. Boroojeni, F. G., B., Svihus, H. G. V., Reichenbach, and J., Zentek. 2016. “The Effects of Hydrothermal Processing on Feed Hygiene, Nutrient Availability, Intestinal Microbiota and Morphology in Poultry-A Review.” Animal Feed Science and Technology 220: 187–215. doi:10.1016/j.anifeedsci.2016.07.010.
10. Camire, M. E., 1991. “Protein Functionality Modification by Extrusion Cooking.” Journal of the American Oil Chemists’ Society 68 (3): 200–205. doi:10.1007/BF02657770.
11. Carbonaro, M., M., Cappelloni, S., Nicoli, M., Lucarini, and E., Carnovale. 1997. “Solubility-Digestibility Relationship of Legume Proteins.” Journal of Agricultural and Food Chemistry 45: 3387–3394. doi:10.1021/jf970070y.
12. Cerami, A., 1985. “Hypothesis. Glucose as a Mediator of Aging.” Journal of the American Geriatrics Society 33: 626–634. doi:10.1111/jgs.1985.33.issue-9.
13. Chao, C. C., Y. S., Ma, and E. R., Stadtman. 1997. “Modification of Protein Surface Hydrophobicity and Methionine Oxidation by Oxidative Systems.” Proceedings of the National Academy of Sciences of the United States of America 94: 2969–2974. doi:10.1073/pnas.94.7.2969.
14. Chen, N., M., Zhao, and W., Sun. 2013. “Effect of Protein Oxidation on the in Vitro Digestibility of Soy Protein Isolate.” Food Chemistry 141: 3224–3229. doi:10.1016/j.foodchem.2013.05.113.
15. Chen, X., Y. P., Chen, D. W., Wu, C., Wen, and Y. M., Zhou. 2015. “Effects of Heat-Oxidized Soy Protein Isolate on Growth Performance and Digestive Function of Broiler Chickens at Early Age.” Asian-Australasian Journal of Animal Science 28: 544–550. doi:10.5713/ajas.14.0609.
16. Cucu, T., B., Devreese, B., Kerkaert, F., Mestdagh, M., Sucic, V. I., De Perre, and B., De Meulenaer. 2013. “A Comparative Study of Lipid and Hypochlorous Acid Induced Oxidation of Soybean Proteins.” LWT-Food Science and Technology 50: 451–458. doi:10.1016/j.lwt.2012.08.027.
17. De Marco, M., S., Martínez, F., Hernandez, J., Madrid, F., Gai, L., Rotolo, M., Belforti, et al. 2015. “Nutritional Value of Two Insect Larval Meals (Tenebrio Molitor and Hermetia Illucens) for Broiler Chickens: Apparent Nutrient Digestibility, Apparent Ileal Amino Acid Digestibility and Apparent Metabolizable Energy.” Animal Feed Science and Technology 209: 211–218. doi:10.1016/j.anifeedsci.2015.08.006.
18. Degenhardt, T. P., S. R., Thorpe, and J. W., Baynes. 1998. “Chemical Modification of Proteins by Methylglyoxal.” Cellular & Molecular Biology 44: 1139–1145.
19. Dong, X. Y., M. M. M., Azzam, W., Rao, D. Y., Yu, and X. T., Zou. 2012. “Evaluating the Impact of Excess Dietary Tryptophan on Laying Performance and Immune Function of Laying Hens Reared under Hot and Humid Summer Conditions.” British Poultry Science 53: 491–496. doi:10.1080/00071668.2012.719149.
20. Ellman, G. L., 1959. “Tissue Sulfhydryl Groups.” Archives of Biochemistry and Biophysics 82: 70–77. doi:10.1016/0003-9861(59)90090-6.
21. Fu, S. L., and R. T., Dean. 1997. “Structural Characterization of the Products of Hydroxyl-Radical Damage to Leucine and Their Detection on Proteins.” Biochemical Journal 324: 41–48. doi:10.1042/bj3240041.
22. Giri, S. S., S. K., Sahoo, A. K., Sahu, and P. K., Mukhopadhyay. 2000. “Nutrient Digestibility and Intestinal Enzyme Activity of Clarias Batrachus (Linn.) Juveniles Fed on Dried Fish and Chicken Viscera Incorporated Diets.” Bioresource Technology 71: 97–101. doi:10.1016/S0960-8524(99)90072-X.
23. Goebel, K. P., and H. H., Stein. 2011. “Ileal Digestibility of Amino Acids in Conventional and low-Kunitz Soybean Products Fed to Weanling Pigs. Asian-Australas.” Journal of Animal Science 24: 88–95.
24. González-Vega, J. C., B. G., Kim, J. K., Htoo, A., Lemme, and H. H., Stein. 2011. “Amino Acid Digestibility in Heated Soybean Meal Fed to Growing Pigs.” Journal of Animal Science 89: 3617–3625. doi:10.2527/jas.2010-3465.
25. Gravador, R. S., S., Jongberg, M. L., Andersen, G., Luciano, A., Priolo, and M. N., Lund. 2014. “Dietary Citrus Pulp Improves Protein Stability in Lamb Meat Stored under Aerobic Conditions.” Meat Science 97: 231–236. doi:10.1016/j.meatsci.2014.01.016.
26. Huang, Y., Y., Hua, and A., Qiu. 2006. “Soybean Protein Aggregation Induced by Lipoxygenase Catalyzed Linoleic Acid Oxidation.” Food Research International 39: 240–249. doi:10.1016/j.foodres.2005.07.012.
27. Kim, J. G., F., Sabbagh, N., Santanam, J. N., Wilcox, R. M., Medford, and S., Parthasarathy. 1997. “Generation of a Polyclonal Antibody against Lipid Peroxide-Modified Proteins.” Free Radical Biology & Medicine 23: 251–259. doi:10.1016/S0891-5849(96)00615-6.
28. Levine, R. L., D., Garland, C. N., Oliver, A., Amici, I., Climent, A. G., Lenz, B. W., Ahn, S., Shaltiel, and E. R., Stadtman. 1990. “Determination of Carbonyl Content in Oxidatively Modified Proteins.” Methods in Enzymology 186: 464–478.
29. Levine, R. L., and E. R., Stadtman. 2001. “Oxidative Modification of Proteins during Aging.” Experimental Gerontology 36: 1495–1502. doi:10.1016/S0531-5565(01)00135-8.
30. Liang, J. H., 1999. “Fluorescence Due to Interactions of Oxidizing Soybean Oil and Soybean Proteins.” Food Chemistry 66: 103–108. doi:10.1016/S0308-8146(98)00250-7.
31. Liener, I. E., 1994. “Implications of Antinutritional Components in Soybean Foods.” Critical Reviews in Food Science & Nutrition 34: 31–67. doi:10.1080/10408399409527649.
32. Liu, G., Y. L., Xiong, and D. A., Butterfield. 2000. “Chemical, Physical, and Gel-Forming Properties of Oxidized Myofibrils and Whey-And Soybean-Protein Isolates.” Journal of Food Science 65: 811–818. doi:10.1111/j.1365-2621.2000.tb13592.x.
33. Mccarthy, J. F., F. X., Aherne, and D. B., Okai. 1974. “Use of HCl Insoluble Ash as an Index Material for Determining Apparent Digestibility with Pigs.” Canadian Journal of Animal Science 54: 107–109. doi:10.4141/cjas74-016.
34. Purushotham, B., P. M., Radhakrishna, and B. S., Sherigara. 2007. “Effects of Steam Conditioning and Extrusion Temperature on Some Antinutritional Factors of Soyabean (Glycine Max) for Pet Food Applications.” American Journal of Animal and Veterinary Sciences 2: 1–5. doi:10.3844/ajavsp.2007.1.5.
35. Ravindran, V., M. R., Abdollahi, and S. M., Bootwalla. 2014. “Nutrient Analysis, Metabolizable Energy, and Digestible Amino Acids of Soybean Meals of Different Origins for Broilers.” Poultry Science 93: 2567–2577. doi:10.3382/ps.2014-04068.
36. Saeed, S., D., Gillies, G., Wagner, and N. K., Howell. 2006. “ESR and NMR Spectroscopy Studies on Protein Oxidation and Formation of Dityrosine in Emulsions Containing Oxidised Methyl Linoleate.” Food and Chemical Toxicology 44: 1385–1392. doi:10.1016/j.fct.2006.03.005.
37. Santé-Lhoutellier, V., E., Engel, L., Aubry, and P., Gatellier. 2008b. “Effect of Animal (Lamb) Diet and Meat Storage on Myofibrillar Protein Oxidation and in Vitro Digestibility.” Meat Science 79: 777–783. doi:10.1016/j.meatsci.2007.11.011.
38. Santé-Lhoutellier, V., L., Aubry, and P., Gatellier. 2007. “Effect of Oxidation on in Vitro Digestibility of Skeletal Muscle.” Journal of Agricultural and Food Chemistry 55: 5343–5348. doi:10.1021/jf070252k.
39. Santé-Lhoutellier, V., T., Astruc, P., Marinova, E., Greve, and P., Gatellier. 2008a. “Effect of Meat Cooking on Physicochemical State and in Vitro Digestibility of Myofibrillar Proteins.” Journal of Agricultural and Food Chemistry 56: 1488–1494. doi:10.1021/jf072999g.
40. Schwert, G. W., and Y., Takenaka. 1955. “A Spectrophotometric Determination of Trypsin and Chymotrypsin.” Biochimica Et Biophysica Acta 16: 570–575. doi:10.1016/0006-3002(55)90280-8.
41. Selle, P. H., S. Y., Liu, J., Cai, and A. J., Cowieson. 2012. “Steam-Pelleting and Feed Form of Broiler Diets Based on Three Coarsely Ground Sorghums Influences Growth Performance,Nutrient Utilisation, Starch and Nitrogen Digestibility.” Animal Production Science 52: 842–852. doi:10.1071/AN12026.
42. Shacter, E., 2000. “Quantification and Significance of Protein Oxidation in Biological Samples.” Drug Metabolism Reviews 32: 307–326. doi:10.1081/DMR-100102336.
43. Somogyi, M., 1960. “Modifications of Two Methods for the Assay of Amylase.” Clinical Chemistry 6: 23–35.
44. SPSS. 2008. SPSS 16.0 for Windows. Chicago, IL: SPSS Inc.
45. Stadtman, E. R., 2006. “Protein Oxidation and Aging.” Free Radical Research 40: 1250–1258. doi:10.1080/10715760600918142.
46. Tang, X., Q., Wu, G., Le, J., Wang, K., Yin, and Y., Shi. 2012a. “Structural and Antioxidant Modification of Wheat Peptides Modified by the Heat and Lipid Peroxidation Product Malondialdehyde.” Journal of Food Science 77: H16–22. doi:10.1111/j.1750-3841.2011.02500.x.
47. Tang, X., Q., Wu, G., Le, and Y., Shi. 2012b. “Effects of Heat Treatment on Structural Modification and in Vivo Antioxidant Capacity of Soybean Protein.” Nutrition 28: 1180–1185. doi:10.1016/j.nut.2012.03.011.
48. Tironi, V. A., L. B., Lopez, N., Pellegrino, M. C., Añtón, and M. C., Tomás. 2004. “Malonaldehyde-Induced Microstructural Modifications in Myofibrillar Proteins of Sea Salmon (Pseudopercis Semifasciata).” Journal of Food Science 69: 519–523. doi:10.1111/j.1365-2621.2004.tb13645.x.
49. Verduin, P. A., J. M. H. M., Punt, and H. H., Kreutzer. 1973. “Studies on the Determination of Lipase Activity.” Clinica Chimica Acta 46: 11–19. doi:10.1016/0009-8981(73)90096-X.
50. Wang, B. W., and Y. L., Xiong. 1998. “Functional Stability of Antioxidant-Washed, Cryoprotectant-Treated Beef Heart Surimi during Frozen Storage.” Journal of Food Science 63: 293–298. doi:10.1111/j.1365-2621.1998.tb15729.x.
51. Wen, C., L. C., Wang, Y. M., Zhou, Z. Y., Jiang, and T., Wang. 2012. “Effect of Enzyme Preparation on Egg Production, Nutrient Retention, Digestive Enzyme Activities and Pancreatic Enzyme Messenger RNA Expression of Late-Phase Laying Hens.” Animal Feed Science and Technology 172: 180–186. doi:10.1016/j.anifeedsci.2011.11.012.
52. Wu, D. W., X., Chen, X., Yang, Z. X., Leng, P. S., Yan, and Y. M., Zhou. 2014. “Effects of Heat Treatment of Soy Protein Isolate on the Growth Performance and Immune Function of Broiler Chickens.” Poultry Science 93: 326–334. doi:10.3382/ps.2013-03507.
53. Wu, W., C., Zhang, X., Kong, and Y., Hua. 2009. “Oxidative Modification of Soybean Protein by Peroxyl Radicals.” Food Chemistry 116: 295–301. doi:10.1016/j.foodchem.2009.02.049.
54. Wu, W., X., Wu, and Y., Hua. 2010. “Structural Modification of Soy Protein by the Lipid Peroxidation Product Acrolein.” LWT-Food Science and Technology 43: 133–140. doi:10.1016/j.lwt.2009.05.006.
55. Xie, M., L., Zhang, Z. G., Wen, J., Tang, W., Huang, and S. S., Hou. 2014. “Threonine Requirement of White Pekin Ducks from Hatch to 21 D of Age.” British Poultry Science 55: 553–557. doi:10.1080/00071668.2014.929638.
56. Zheng, L., J., Ren, G., Su, B., Yang, and M., Zhao. 2013. “Comparison of in Vitro Digestion Characteristics and Antioxidant Activity of Hot-And Cold-Pressed Peanut Meals.” Food Chemistry 141: 4246–4252. doi:10.1016/j.foodchem.2013.06.081.
57. Zhu, C. P., X. C., Zhai, L. Q., Li, X. X., Wu, and B., Li. 2015. “Response Surface Optimization of Ultrasound-Assisted Polysaccharides Extraction from Pomegranate Peel.” Food Chemistry 177: 139–146. doi:10.1016/j.foodchem.2015.01.022.
58. Zirlin, A., and M., Karel. 1969. “Oxidation Effects in a Freeze-Dried Gelatin-Methyl Linoleate System.” Journal of Food Science 34: 160–165. doi:10.1111/jfds.1969.34.issue-2.