Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE (Open Access)

Comparative performance of broiler chickens offered nutritionally equivalent diets based on six diverse, ‘tannin-free’ sorghum varieties with quantified concentrations of phenolic compounds, kafirin, and phytate

Ha H. Truong A B , Karlie A. Neilson C , Bernard V. McInerney C , Ali Khoddami D , Thomas H. Roberts D , David J. Cadogan E , Sonia Yun Liu A and Peter H. Selle A F
+ Author Affiliations
- Author Affiliations

A Poultry Research Foundation within the Faculty of Veterinary Science, The University of Sydney, 425 Werombi Road, Camden, NSW 2570, Australia.

B Poultry CRC, University of New England, Armidale, NSW 2351, Australia.

C Australian Proteome Analysis Facility, Macquarie University, Sydney, NSW 2109, Australia.

D Faculty of Agriculture and Environment, The University of Sydney, NSW 2006, Australia.

E Feedworks Pty Ltd, Romsey, Vic. 3434, Australia.

F Corresponding author. Email: peter.selle@sydney.edu.au

Animal Production Science 57(5) 828-838 https://doi.org/10.1071/AN16073
Submitted: 8 February 2016  Accepted: 9 February 2016   Published: 1 June 2016

Journal Compilation © CSIRO Publishing 2017 Open Access CC BY-NC-ND

Abstract

Starch is the main source of energy in sorghum-based diets but starch/energy utilisation by broiler chickens offered these diets may be substandard. Both in vitro and in vivo data indicate that the digestibility of sorghum starch is inferior to that of other feed grains, especially maize. Three ‘starch-extrinsic’ factors in grain sorghum, namely ‘non-tannin’ phenolic compounds, kafirin and phytate may negatively influence starch/energy utilisation in sorghum-based broiler diets. To test this hypothesis, concentrations of polyphenols, free, bound and conjugated phenolic acids, kafirin and phytate were quantified in six diverse ‘tannin-free’ (Type I) grain sorghum varieties. These sorghums were incorporated into nutritionally equivalent diets at 620 g/kg and offered to male broiler chickens from 7 to 28 days post-hatch. Growth performance, nutrient utilisation (AME, ME : GE ratios, N retention, AMEn) and starch and protein (N) digestibility coefficients and disappearance rates in four small intestinal segments were determined. Numerous relationships that were either significant (P < 0.05), or approached significance (P < 0.10), were detected that indicated various ‘non-tannin’ phenolic compounds, kafirin and phytate in sorghums negatively influenced nutrient utilisation parameters in broiler chickens. ME : GE ratios are sensitive indicators of efficiency of energy utilisation and were most negatively influenced by flavan-4-ols (r = –0.919; P < 0.015), which are polyphenolic compounds. Moreover, flavan-4-ols in tandem with conjugated vanillic acid negatively influenced (r = –0.993; P < 0.005) ME : GE ratios on the basis of a valid multiple linear regression. Similarly, conjugated vanillic and bound ferulic acids in tandem negatively influenced AME (r = –0.990; P < 0.005). N retention was most negatively influenced by kafirin (r = –0.887; P < 0.025). Thus, it appears that both phenolic compounds and kafirin may have deleterious effects on nutrient utilisation of sorghum-based broiler diets and recommendations are made that should enhance the quality of sorghum as a feedstuff for chicken-meat production based on these findings.

Additional keywords: condensed tannin, conjugated and bound phenolic acids, ferulic acid, free, polyphenols.


References

Barros F, Awika JM, Rooney LW (2012) Interaction of tannins and other sorghum phenolic compounds with starch and effects on in vitro starch digestibility. Journal of Agricultural and Food Chemistry 60, 11 609–11 617.
Interaction of tannins and other sorghum phenolic compounds with starch and effects on in vitro starch digestibility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1WltrjO&md5=5403419372f42fec28e8df08fcbc959eCAS |

Beta T, Corke H (2004) Effect of ferulic acid and catechin on sorghum and maize starch pasting properties. Cereal Chemistry 81, 418–422.
Effect of ferulic acid and catechin on sorghum and maize starch pasting properties.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjvFelt7o%3D&md5=7ed0a9785c98b94df6695ba728992316CAS |

Black JL, Hughes RJ, Nielsen SG, Tredrea AM, MacAlpine R, Van Barneveld RJ (2005) The energy value of cereal grains, particularly wheat and sorghum, for poultry. Proceedings of the Australian Poultry Science Symposium 17, 21–29.

Chandrashekar A, Kirleis A (1998) Influence of protein on starch gelatinization in sorghum. Cereal Chemistry 65, 457–462.

de Mesa-Stonestreet NJ, Alavi S, Bean SR (2010) Sorghum proteins: the concentration, isolation, modification, and food applications of kafirins. Journal of Food Science 75, 90–104.

Giuberti G, Gallo A, Cerioli C, Masoero F (2012) In vitro starch digestion and predicted glycemic index of cereal grains commonly utilized in pig nutrition. Animal Feed Science and Technology 174, 163–173.
In vitro starch digestion and predicted glycemic index of cereal grains commonly utilized in pig nutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XkvF2ju7w%3D&md5=a8d42d856d56793a7317f170460293bdCAS |

Hamaker BR, Mohamed AA, Habben JE, Huang CP, Larkins BA (1995) Efficient procedure for extracting maize and sorghum kernel proteins reveals higher prolamin contents than conventional method. Cereal Chemistry 72, 583–588.

Hill FW, Anderson DL (1958) Comparison of metabolisable energy and productive energy deerminations with growing chicks. The Journal of Nutrition 64, 587–603.

Hung PV, Phat NH, Phi NTL (2013) Physicochemical properties and antioxidant capacity of debranched starch-ferulic acid complexes. Stärke 65, 382–389.

Kandil A, Li J, Vasanthan T, Bressler DC (2012) Phenolic acids in some cereal grains and their inhibitory effect on starch liquefaction and saccharification. Journal of Agricultural and Food Chemistry 60, 8444–8449.
Phenolic acids in some cereal grains and their inhibitory effect on starch liquefaction and saccharification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVaktrzL&md5=5f83ace6824283756b34650a3cc1119dCAS | 22793673PubMed |

Khoddami A, Truong HH, Liu SY, Roberts TH, Selle PH (2015) Concentrations of specific phenolic compounds in six red sorghums influence nutrient utilisation in broilers. Animal Feed Science and Technology
Concentrations of specific phenolic compounds in six red sorghums influence nutrient utilisation in broilers.Crossref | GoogleScholarGoogle Scholar |

Liu SY, Fox G, Khoddami A, Neilsen KA, Truong HH, Moss AF, Selle PH (2015) Grain sorghum: a conundrum for chicken-meat production. Agriculture 5, 1224–1251.
Grain sorghum: a conundrum for chicken-meat production.Crossref | GoogleScholarGoogle Scholar |

Mahasukhonthachat K, Sopade PA, Gidley MJ (2010) Kinetics of starch digestion and functional properties of twin-screw extruded sorghum. Journal of Cereal Science 51, 392–401.
Kinetics of starch digestion and functional properties of twin-screw extruded sorghum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmsVeksrg%3D&md5=c0420e99504f876534a4a43ff11c3653CAS |

Nyachoti CM, Atkinson JL, Leeson S (1997) Sorghum tannins: a review. World’s Poultry Science Journal 53, 5–21.
Sorghum tannins: a review.Crossref | GoogleScholarGoogle Scholar |

Rooney LW, Pflugfelder RL (1986) Factors affecting starch digestibility with special emphasis on sorghum and corn. Journal of Animal Science 63, 1607–1623.

Salinas I, Pro A, Salinas Y, Sosa E, Becerril CM, Cuca M, Cervantes M, Gallegos J (2006) Compositional variation amongst sorghum hybrids: effect of kafirin concentration on metabolizable energy. Journal of Cereal Science 44, 342–346.
Compositional variation amongst sorghum hybrids: effect of kafirin concentration on metabolizable energy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtF2qu7%2FM&md5=67085bd131060fce8f620da6cd788118CAS |

Selle PH (2011) The protein quality of sorghum grain. Proceedings of the Australian Poultry Science Symposium 22, 147–156.

Selle PH, Ravindran V (2007) Microbial phytase in poultry nutrition. Animal Feed Science and Technology 135, 1–41.
Microbial phytase in poultry nutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkt1artb8%3D&md5=10c873cc2a2fa70b4c8c35c36f7ce39aCAS |

Selle PH, Walker AR, Bryden WL (2003) Total and phytate-phosphorus contents and phytase activity of Australian-sourced feed ingredients for pigs and poultry. Australian Journal of Experimental Agriculture 43, 475–479.
Total and phytate-phosphorus contents and phytase activity of Australian-sourced feed ingredients for pigs and poultry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlslOnsbY%3D&md5=a74bd3ec461d75175387cae678b82441CAS |

Selle PH, Cadogan DJ, Li X, Bryden WL (2010) Implications of sorghum in broiler chicken nutrition. Animal Feed Science and Technology 156, 57–74.
Implications of sorghum in broiler chicken nutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjtVCksr4%3D&md5=80de3bfba630d56db0d6e23cc497213aCAS |

Selle PH, Cowieson AJ, Cowieson NP, Ravindran V (2012) Protein-phytate interactions in pig and poultry nutrition; a reappraisal. Nutrition Research Reviews 25, 1–17.
Protein-phytate interactions in pig and poultry nutrition; a reappraisal.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpvVOisb0%3D&md5=0d23dafc48ae2e0b3549e3f327eecb1eCAS | 22309781PubMed |

Selle PH, Liu SY, Cowieson AJ (2013) Sorghum: an enigmatic grain for chicken-meat production. In ‘Sorghum: production, growth habits and health benefits’. (Ed. PC Parra) pp. 1–44. (Nova Publishers Inc.: Hauppauge, NY)

Siriwan P, Bryden WL, Mollah Y, Annison EF (1993) Measurement of endogenous amino-acid losses in poultry. British Poultry Science 34, 939–949.
Measurement of endogenous amino-acid losses in poultry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXivFOgsLg%3D&md5=9cf977713d25c4cadedec9959d9ad230CAS | 8156432PubMed |

Taylor JRN (2005) Non-starch polysaccharides, proteins and starch: form function and feed – highlight on sorghum. Proceedings of the Australian Poultry Science Symposium 17, 10–16.

Taylor JRN, Schüssler L, van der Walt WH (1984) Fractionation of proteins from low-tannin sorghum grain. Journal of Agricultural and Food Chemistry 32, 149–154.
Fractionation of proteins from low-tannin sorghum grain.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2c7mtlSjtQ%3D%3D&md5=073418d78cde38667f788919652ebb68CAS |

Thompson LU, Yoon JH (1984) Starch digestibility as affected by polyphenols and phytic acid. Journal of Food Science 49, 1228–1229.
Starch digestibility as affected by polyphenols and phytic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXlvFSjsbo%3D&md5=f6ef04cc67bf363063a94bcb1a7dc92aCAS |

Thompson LU, Yoon JH, Jenkins DJA, Wolever TMS, Jenkins AL (1983) Relationships between polyphenol intake and blood glucose response in normal and diabetic individuals. The American Journal of Clinical Nutrition 39, 745–751.

Tomasik P, Schilling CH (1998) Complexes of starch with organic guests. Advances in Carbohydrate Chemistry and Biochemistry 53, 345–426.
Complexes of starch with organic guests.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkvFCg&md5=bb6439b63b20fef7f2c2b6b8954fbbdaCAS |

Truong HH, Neilson KA, McInerney BV, Khoddami A, Roberts TH, Liu SY, Selle PH (2015a) Performance of broiler chickens offered nutritionally-equivalent diets based on two red grain sorghums with quantified kafirin concentrations as intact pellets or reground mash following steam-pelleting at 65 or 97°C conditioning temperatures. Animal Nutrition 1, 220–228.
Performance of broiler chickens offered nutritionally-equivalent diets based on two red grain sorghums with quantified kafirin concentrations as intact pellets or reground mash following steam-pelleting at 65 or 97°C conditioning temperatures.Crossref | GoogleScholarGoogle Scholar |

Truong HH, Bold RM, Liu SY, Selle PH (2015b) Standard phytase inclusion in maize-based broiler diets enhances digestibility coefficients of starch, amino acids and sodium in four small intestinal segments and digestive dynamics of starch and protein. Animal Feed Science and Technology 209, 240–248.
Standard phytase inclusion in maize-based broiler diets enhances digestibility coefficients of starch, amino acids and sodium in four small intestinal segments and digestive dynamics of starch and protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsFeitLrJ&md5=b7798a72548136930b704fba49f5a138CAS |

Truong HH, Liu SY, Selle PH (2016) Starch utilisation in chicken-meat production: the foremost factors. Animal Production Science 56, 797–814.

Wallace JC, Lopes MA, Palva E, Larkins BA (1990) New methods for extraction and quantitation of zeins reveal a high content of γ-zein in modified opaque-2 maize. Plant Physiology 92, 191–196.
New methods for extraction and quantitation of zeins reveal a high content of γ-zein in modified opaque-2 maize.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXpslWhsA%3D%3D&md5=48f8114f128f953a07da61bb9a0bfec0CAS | 16667246PubMed |

Waniska RD, Hugo LF, Rooney LW (1992) Practical methods to determine the presence of tannins in sorghum. Journal of Applied Poultry Research 1, 122–128.
Practical methods to determine the presence of tannins in sorghum.Crossref | GoogleScholarGoogle Scholar |

Welsch CA, Lachance PA, Wasserman BP (1989) Dietary phenolic compounds: inhibition of Na+-dependent d-glucose uptake in rat intestinal brush border membrane vesicles. The Journal of Nutrition 119, 1698–1704.

Wong JH, Marx DB, Wilson JD, Buchanan BB, Lemaux PG, Pedersen JF (2010) Principal component analysis and biochemical characterization of protein and starch reveal primary targets for improving sorghum grain. Plant Science 179, 598–611.
Principal component analysis and biochemical characterization of protein and starch reveal primary targets for improving sorghum grain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlKht7jK&md5=2cbb2f708586ae0895512b992284a11cCAS |

Yu J, Vasanthan T, Temelli F (2001) Analysis of phenolic acids in barley by high-performance liquid chromatography. Journal of Agricultural and Food Chemistry 49, 4352–4358.
Analysis of phenolic acids in barley by high-performance liquid chromatography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmtVWktLo%3D&md5=11a308512661364e31724d5e491f1f65CAS | 11559137PubMed |

Zhu F (2015) Interactions between starch and phenolic compound. Trends in Food Science & Technology 43, 129–143.
Interactions between starch and phenolic compound.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjs1ajsL0%3D&md5=5bb08110c768bb1f77cf81b94e689870CAS |