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RESEARCH ARTICLE

Interactive effects of dietary protein concentration, a mono-component exogenous protease and ascorbic acid on broiler performance, nutritional status and gut health

A. J. Cowieson A C , F. Zaefarian B , I. Knap A and V. Ravindran B
+ Author Affiliations
- Author Affiliations

A DSM Nutritional Products, Wurmisweg 576, Kaiseraugst, Switzerland.

B Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North 4442, New Zealand.

C Corresponding author. Email: aaron.cowieson@dsm.com

Animal Production Science 57(6) 1058-1068 https://doi.org/10.1071/AN15740
Submitted: 21 October 2015  Accepted: 20 March 2016   Published: 29 July 2016

Abstract

A total of 640 male Ross 308 broiler chickens were used to explore the interactive effects of diet nutrient density, exogenous protease and ascorbic acid on performance, nutrient digestibility and various gut health metrics. A total of eight dietary treatments were arranged as a 2 × 2 × 2 factorial with the factors being adequate or reduced (~4%) crude protein and amino acids, without or with exogenous protease and without or with supplemental ascorbic acid. Over the 35-day experimental period, birds that received the adequate diet had higher (P < 0.01) bodyweight gain and lower (P < 0.001) feed conversion ratio (FCR) than birds that received the diet with reduced protein and amino acid density. Supplemental protease reduced (P < 0.001) FCR and this influence was more apparent in birds fed the diet with reduced protein concentration. Gut tensile strength tended to be increased by protease (P = 0.09) and ascorbic acid (P = 0.06) supplementation. Supplemental protease reduced (P < 0.001) jejunal goblet cell numbers and epithelial thickness and increased (P < 0.05) villus height compared with unsupplemented diets. Ascorbic acid tended (P = 0.05) to increase sialic acid concentration in ileal digesta. Protease increased (P < 0.01) the coefficients of apparent ileal digestibility for all amino acids other than methionine and this effect tended (P = 0.07 to 0.09) to be more pronounced in the low protein diet for aspartic acid, histidine and arginine. The concentration of taurine in ileal digesta was reduced (P < 0.01) by protease whereas hydroxyproline concentrations tended (P = 0.09) to increase by ascorbic acid addition. These results confirm previous reports on the effectiveness of exogenous protease in diets reduced in crude protein and digestible amino acids. Furthermore, both protease and ascorbic acid may influence gut health through promotion of tensile strength, epithelial morphology and endogenous protein flow. The interaction between exogenous protease and ascorbic acid on gut health with an emphasis on collagen structure and tight junction integrity is an area for future study.

Additional keywords: broiler chicken, nutrition.


References

Angel CR, Saylor W, Vieira SL, Ward N (2011) Effects of a monocomponent protease on performance and protein utilization in 7- to 22-day-old broiler chickens. Poultry Science 90, 2281–2286.
Effects of a monocomponent protease on performance and protein utilization in 7- to 22-day-old broiler chickens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlGrsb%2FK&md5=bd900c406d908223afafdaa591e1cbd8CAS | 21934011PubMed |

AOAC (2005) ‘Official methods of analysis.’ 18th edn. (Association of Official Analytical Chemists: Washington, DC)

Bilgili SF, Hess JB (1997) Tensile strength of broiler intestine as influenced by age and feed withdrawal. Journal of Applied Poultry Research 6, 279–283.
Tensile strength of broiler intestine as influenced by age and feed withdrawal.Crossref | GoogleScholarGoogle Scholar |

Bregendahl K, Sell JL, Zimmerman DR (2002) Effect of low-protein diets on growth performance and body composition of broiler chicks. Poultry Science 81, 1156–1167.
Effect of low-protein diets on growth performance and body composition of broiler chicks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XntVCjtr4%3D&md5=8da92b49ae75a828074df54b7ca58570CAS | 12211308PubMed |

Cowieson AJ, Roos FF (2014) Bioefficacy of a mono-component protease in the diets of pigs and poultry: a meta-analysis of effect on ileal amino acid digestibility. Journal of Applied Animal Nutrition 2, e13
Bioefficacy of a mono-component protease in the diets of pigs and poultry: a meta-analysis of effect on ileal amino acid digestibility.Crossref | GoogleScholarGoogle Scholar |

Cowieson AJ, Lu H, Ajuwon KM, Adeola O (2016) Interactive effects of dietary protein source and exogenous protease on growth performance, immune competence and jejunal health of broiler chickens. Animal Production Science
Interactive effects of dietary protein source and exogenous protease on growth performance, immune competence and jejunal health of broiler chickens.Crossref | GoogleScholarGoogle Scholar |

Doan BH (2000) Effects of different levels of dietary calcium and supplemental vitamin C on growth, survivability, leg abnormalities, total ash in the tibia, serum calcium and phosphorus in 0–4 week old chicks under tropical conditions. Livestock Research for Rural Development 12, 1–4.

Doan BH, Giang VD (1998) Effects of vitamin C supplementation of a diet for 0–4 week old chicks on the absorption of calcium and phosphorus. Agricultura Tropica et Subtropica 31, 117–121.

Farquharson C, Berry JL, Mawer EB, Seawright E, Whitehead CC (1998) Ascrobic acid-induced chondrocyte differentiation: the role of the extracellular matrix and 1,25-dihydroxycholecalciferol. European Journal of Cell Biology 76, 110–118.
Ascrobic acid-induced chondrocyte differentiation: the role of the extracellular matrix and 1,25-dihydroxycholecalciferol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktVKltb0%3D&md5=c63ed0a59323a984929b3f2b64d86095CAS | 9696350PubMed |

Freitas DM, Vieira SL, Angel CR, Favero A, Maiorka A (2011) Performance and nutrient utilization of broilers fed diets supplemented with a novel mono-component protease. Journal of Applied Poultry Research 20, 322–334.
Performance and nutrient utilization of broilers fed diets supplemented with a novel mono-component protease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Cks7rL&md5=8b79835c5882ea85baf9f2fb242fc63fCAS |

Fru-Nji F, Kluenter A-M, Fischer M, Pontoppidan K (2011) A feed serine protease improves broiler performance and increases protein and energy digestibility. Japanese Poultry Science 48, 239–246.
A feed serine protease improves broiler performance and increases protein and energy digestibility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1Slt77P&md5=af73024b2354b6ecfb2aa909d8f66346CAS |

Fry SC (1998) Oxidative scission of plant cell wall polysaccharides by ascorbic acid-induced free radicals. Biochemical Journal 12, 2087–2093.

Gal-Garber O, Mabjeesh SJ, Sklan D, Uni Z (2003) Nutrient transport in the small intestine: Na+,K+-ATPase expression and activity in the small intestine of the chicken as influenced by dietary sodium. Poultry Science 82, 1127–1133.
Nutrient transport in the small intestine: Na+,K+-ATPase expression and activity in the small intestine of the chicken as influenced by dietary sodium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmsVWkt7k%3D&md5=40fe4d41e5279770e7e591853e525d50CAS | 12872969PubMed |

Ghazi S, Rooke JA, Galbraith H, Bedford MR (2002) The potential for the improvement of the nutritive value of soya-bean meal by different proteases in broiler chicks and broiler cockerels. British Poultry Science 43, 70–77.
The potential for the improvement of the nutritive value of soya-bean meal by different proteases in broiler chicks and broiler cockerels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjt1ymtbs%3D&md5=b572fb0e39e149fda84ceb8ceeb29394CAS | 12003341PubMed |

Gous RM, Morris TR (2005) Nutritional interventions in alleviating the effects of high temperatures in broiler production. World’s Poultry Science Journal 61, 463–475.
Nutritional interventions in alleviating the effects of high temperatures in broiler production.Crossref | GoogleScholarGoogle Scholar |

Granot I, Bartov I, Plavnik I, Wax E, Hurwitz S, Pines M (1991) Increased skin tearing in broilers and reduced collagen synthesis in skin in vivo and in vitro in response to the coccidiostat halofuginone. Poultry Science 70, 1559–1563.
Increased skin tearing in broilers and reduced collagen synthesis in skin in vivo and in vitro in response to the coccidiostat halofuginone.Crossref | GoogleScholarGoogle Scholar | 1886867PubMed |

He L, Wu L, Xu Z, Li T, Yao K, Cui Z, Yin Y, Wu G (2015) Low-protein diets affect ileal amino acid digestibility and gene expression of digestive enzymes in growing and finishing pigs. Amino Acids
Low-protein diets affect ileal amino acid digestibility and gene expression of digestive enzymes in growing and finishing pigs.Crossref | GoogleScholarGoogle Scholar | 26210756PubMed |

Huang C, Guo Y, Yuan J (2014) Dietary taurine impairs intestinal growth and mucosal structure of broiler chickens by increasing toxic bile acid concentrations in the intestine. Poultry Science 93, 1475–1483.
Dietary taurine impairs intestinal growth and mucosal structure of broiler chickens by increasing toxic bile acid concentrations in the intestine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXpt1Wjsrc%3D&md5=696902d74b877ac0cd94979fb3c09715CAS | 24879697PubMed |

Jourdian GW, Dean L, Roseman S (1971) A periodate-resorcinol method for the quantitative estimation of free sialic acids and their glycosides. The Journal of Biological Chemistry 246, 430–435.

Kalmendal R, Tauson R (2012) Effects of a xylanase and protease, individually or in combination, and an ionophore coccidiostat on performance, nutrient utilization, and intestinal morphology in broiler chickens fed a wheat-soybean meal-based diet. Poultry Science 91, 1387–1393.
Effects of a xylanase and protease, individually or in combination, and an ionophore coccidiostat on performance, nutrient utilization, and intestinal morphology in broiler chickens fed a wheat-soybean meal-based diet.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpsVKisL4%3D&md5=b24e42ad49207fc6a65a2e6050d0864fCAS | 22582297PubMed |

Lambert GP (2004) Role of gastrointestinal permeability in exertional heatstroke. Exercise and Sports Sciences Reviews 32, 185–190.
Role of gastrointestinal permeability in exertional heatstroke.Crossref | GoogleScholarGoogle Scholar |

Liu SY, Selle PH, Court SG, Cowieson AJ (2013) Protease supplementation of sorghum-based broiler diets enhances amino acid digestibility coefficients in four small intestinal sites and accelerates their rates of digestion. Animal Feed Science and Technology 183, 175–183.
Protease supplementation of sorghum-based broiler diets enhances amino acid digestibility coefficients in four small intestinal sites and accelerates their rates of digestion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXovVClur4%3D&md5=80067a08d2d083ed4a8776070d884568CAS |

Marron I, Bedford MR, McCracken KJ (2001) The effects of adding xylanase, vitamin C and copper sulphate to wheat-based diets on broiler performance. British Poultry Science 42, 493–500.
The effects of adding xylanase, vitamin C and copper sulphate to wheat-based diets on broiler performance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnsFSis74%3D&md5=1130bf94e62ce868a9e9f99d8eb43d05CAS |

Moran ET, Bushong RD, Bilgili SF (1992) Reducing dietary crude protein for broilers while satisfying amino acid requirements by least-cost formulation: live performance, litter composition, and yield of fast-food carcass cuts at six weeks. Poultry Science 71, 1687–1694.
Reducing dietary crude protein for broilers while satisfying amino acid requirements by least-cost formulation: live performance, litter composition, and yield of fast-food carcass cuts at six weeks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlvVKjsA%3D%3D&md5=b3eea857a4bcf57da7dc8c81a90f3209CAS |

Namroud NF, Shivazad M, Zaghari M, Zare Shahneh A (2010) Effects of glycine and glutamic acid supplementation to low protein diets on performance, thyroid function and fat deposition in chickens. South African Journal of Animal Science 40, 238–244.
Effects of glycine and glutamic acid supplementation to low protein diets on performance, thyroid function and fat deposition in chickens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjsFClsw%3D%3D&md5=f92668093bd32b5acde26429940789f8CAS |

Odetallah NH, Wang JJ, Garlich JD, Shih JCH (2003) Keratinase in starter diets improves growth of broiler chicks. Poultry Science 82, 664–670.
Keratinase in starter diets improves growth of broiler chicks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjt1yrt7s%3D&md5=e87ddff5557dada0bd6e9a86972eb407CAS | 12710489PubMed |

Ospina-Rojas IC, Murakami AE, Eyng C, Nunes RV, Duarte CRA, Vargas MD (2012) Commercially available amino acid supplementation of low-protein diets for broiler chickens with different ratios of digestible glycine + serine:lysine. Poultry Science 91, 3148–3155.
Commercially available amino acid supplementation of low-protein diets for broiler chickens with different ratios of digestible glycine + serine:lysine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvFShs7zL&md5=fc3ce08bec1f173ace22b3f8be207a20CAS | 23155025PubMed |

Pardue SL, Thaxton JP (1986) Ascorbic acid in poultry: a review. World’s Poultry Science Journal 42, 107–123.
Ascorbic acid in poultry: a review.Crossref | GoogleScholarGoogle Scholar |

Peek HW, van der Klis JD, Vermeulen B, Landman WJM (2009) Dietary protease can alleviate negative effects of a coccidiosis infection on production performance in broiler chickens. Animal Feed Science and Technology 150, 151–159.
Dietary protease can alleviate negative effects of a coccidiosis infection on production performance in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjvV2msro%3D&md5=bd67690bec7033d6e81e4540921b2b7fCAS |

Ravindran V, Cowieson AJ, Selle PH (2008) Influence of dietary electrolyte balance and microbial phytase on the performance and nutrient utilization of broiler starters fed corn-soy diets. Poultry Science 87, 677–688.
Influence of dietary electrolyte balance and microbial phytase on the performance and nutrient utilization of broiler starters fed corn-soy diets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkslyktb4%3D&md5=1dc405810056aa40aa51ccfd735b2a6aCAS | 18339988PubMed |

Ravindran V, Morel PCH, Rutherfurd SM, Thomas DV (2009) Endogenous flow of amino acids in the avian ileum as influenced by increasing dietary peptide concentrations. British Journal of Nutrition 101, 822–828.
Endogenous flow of amino acids in the avian ileum as influenced by increasing dietary peptide concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktleju7c%3D&md5=204249eb3d5d76359ac84168c834b859CAS | 18662428PubMed |

Rooke JA, Slessor M, Fraser H, Thomson JR (1998) Growth performance and gut function of piglets weaned at four weeks of age and fed protease-treated soya-bean meal. Animal Feed Science and Technology 70, 175–190.
Growth performance and gut function of piglets weaned at four weeks of age and fed protease-treated soya-bean meal.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhtlOmu74%3D&md5=9631abd9b6c25a9974a2cf5e1f6118acCAS |

Ross (2007) ‘Ross 308 broiler: nutrition specification, June 2007.’ (Ross Breeders Limited: Newbridge, Midlothian, Scotland)

SAS Institute (2004) ‘SAS system for Windows. Version 9.1.2.’ (SAS Institute Inc.: Cary, NC)

Short FJ, Gorton P, Wiseman J, Boorman KN (1996) Determination of titanium dioxide added as an inert marker in chicken digestibility studies. Animal Feed Science and Technology 59, 215–221.
Determination of titanium dioxide added as an inert marker in chicken digestibility studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XksFSnu7o%3D&md5=db4722e81ce24cabeb9dc1c24466c0abCAS |

Troche C, Sun X, McElroy AP, Remus J, Novak CL (2007) Supplementation of Avizyme 1502 to corn-soybean meal-wheat diets fed to turkey tom poults: the first fifty-six days of age. Poultry Science 86, 496–502.
Supplementation of Avizyme 1502 to corn-soybean meal-wheat diets fed to turkey tom poults: the first fifty-six days of age.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXls12qt7k%3D&md5=6e6eb5f23806167abb7b34d1c123d220CAS | 17297161PubMed |

Wang H, Guo Y, Shih JCH (2008) Effects of dietary supplementation of keratinase on growth performance, nitrogen retention and intestinal morphology of broiler chickens fed diets with soybean and cottonseed meals. Animal Feed Science and Technology 140, 376–384.
Effects of dietary supplementation of keratinase on growth performance, nitrogen retention and intestinal morphology of broiler chickens fed diets with soybean and cottonseed meals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlvV2ltw%3D%3D&md5=c825c1e44cc2df048ba111788e0e05b1CAS |

Wang D, Piao XS, Zeng ZK, Lu T, Zhang Q, Li PF, Xue LF, Kim SW (2011) Effects of keratinase on performance, nutrient utilization, intestinal morphology, intestinal ecology and inflammatory response of weaned piglets fed diets with different levels of crude protein. Asian-Australasian Journal of Animal Sciences 24, 1718–1728.
Effects of keratinase on performance, nutrient utilization, intestinal morphology, intestinal ecology and inflammatory response of weaned piglets fed diets with different levels of crude protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlKltbY%3D&md5=ecaa053af017119cdda3a479b49bfdb3CAS |

Whitehead CC, Keller T (2003) An update on ascorbic acid in poultry. World’s Poultry Science Journal 59, 161–184.
An update on ascorbic acid in poultry.Crossref | GoogleScholarGoogle Scholar |

Windey K, De Preter V, Verbeke K (2012) Relevance of protein fermentation to gut health. Molecular Nutrition & Food Research 56, 184–196.
Relevance of protein fermentation to gut health.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFaru7zI&md5=bb4552133e3833555da5f893062fa5caCAS |

Wu G, Bazer FW, Dai Z, Li D, Wang J, Wu Z (2014) Amino acid nutrition in animals: protein synthesis and beyond. Annual Review of Animal Biosciences 2, 387–417.
Amino acid nutrition in animals: protein synthesis and beyond.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXkt1Sgsrc%3D&md5=000c97e6f51d9c7977b5955f9a0d0b55CAS | 25384149PubMed |

Yuan JM, Wang Z (2010) Effect of taurine on intestinal morphology and utilisation of soy oil in chickens. British Poultry Science 51, 540–545.
Effect of taurine on intestinal morphology and utilisation of soy oil in chickens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1Kgsb7K&md5=e417e3262cd54423a7478326e153319dCAS | 20924849PubMed |