Advertisement

Environmental Science and Pollution Research

, Volume 26, Issue 10, pp 9469–9479 | Cite as

Low digestibility of phytate phosphorus, their impacts on the environment, and phytase opportunity in the poultry industry

  • Farzana Abbasi
  • Tahmina Fakhur-un-Nisa
  • Jingbo Liu
  • Xuegang LuoEmail author
  • Imtiaz Hussain Raja AbbasiEmail author
Review Article
  • 169 Downloads

Abstract

Phosphorus is an essential macro-mineral nutrient for poultry, needed for the body growth, development of bones, genomic function, good quality flesh, and eggs production. The imbalance of organic phosphorus sources in the diet mostly affect the phosphorus digestibility, reduces the poultry performance and health, and increases the environmental pollution burden. A study was reviewed to estimate the low phytate phosphorus digestibility of ingredients in poultry diet and their impacts on environmental ecosystem and opportunity of phytase supplementation. Plant ingredients mostly used in poultry diets are rich in phytate phosphorus. The phytate phosphorus digestibility and utilization is low in the gut of birds which leads to decrease other nutrients digestibility and increase excessive excretion of phosphorus with additional nutrients in the manure. When that manure applied to the lands containing excessive residual phosphorus and additional nutrients which pollute soil, groundwater disturbed the entire ecosystem. This issue is developed by poultry due to lack of digestive enzyme phytase which promotes the phytate phosphorus during digestion and reduces the excessive losses of phosphorus in excreta. To overcome this matter, the addition of mostly exogenous phospho-hydrolytic phytase enzymes in the diet, i.e. Escherichia coli, Peniophora lycii, Aspergillus niger, and Ficum, are the possible ways to increase the digestibility and utilization of phytate phosphorus and promote the stepwise release of phosphorus from phytate and significantly decrease phosphorus excretion. The aim of this review is to highlight the role of phytase supplementation in the poultry feeding, improvement of phytate phosphorus digestibility with performance, and reduction of phosphorus pollution from the environment.

Keywords

Environmental pollution Phytate phosphorus Phytate digestibility Poultry manure Phytase supplementation 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abbasi F, Jingbo L, Hongfu Z, Xiaoyun S, Xuegang L (2018a) Effects of dietary total phosphorus concentration and casein supplementation on the determination of true phosphorus digestibility for broiler chickens. Ital J Anim Sci 17(1):135–144Google Scholar
  2. Abbasi F, Jingbo L, Hongfu Z, Xiaoyun S, Xuegang L (2018b) Effects of feeding corn naturally contaminated with aflatoxin on growth performance, apparent ileal digestibility, serum hormones levels and gene expression of Na+, K+-ATPase in ducklings. Asia Aust J Anim Sci 31(1):91–97Google Scholar
  3. Abbasi IHR, Sahito HA, Abbasi F, Menghwar DR, Kaka NA, Sanjrani MI (2014) Impact of different crude protein levels on growth of lambs under intensive management system. Int J Adv Res 2:227–235Google Scholar
  4. Adedokun S, Owusu AAA, Ragland D, Plumstead P, Adeola O (2015) The efficacy of a new 6-phytase obtained from Buttiauxella spp. Expressed in Trichoderma reesei on digestibility of amino acids, energy, and nutrients in pigs fed a diet based on corn, soybean meal, wheat middlings, and corn distillers’ dried grains with solubles. J Anim Sci 93(1):168–175Google Scholar
  5. Adeola O, Cowieson AJ (2011) Opportunities and challenges in using exogenous enzymes to improve non-ruminant animal production. J Anim Sci 89:3189–3218Google Scholar
  6. Afsharmanesh M, Scott TA, Silversides FG (2008) Effect of wheat type, grinding, heat treatment, and phytase supplementation on growth efficiency and nutrient utilization of wheat-based diets for broilers. Can J Anim Sci 88:57–64Google Scholar
  7. Anderson DM, Gilbert PM, Burkholder JM (2002) Harmful algal blooms and eutrophication: nutrient sources, composition and consequences. Estuaries Coast 25:704–726Google Scholar
  8. Aneja VP, Schlessinger WH, Niyogi D, Jennings G, Gilliam W, Nighton RE, Duke CS, Blunden J, Krishnan S (2006) Emerging national research needs for agricultural air quality. EOS Trans Am Geophys Union 87:25–36Google Scholar
  9. Angel R, Saylor WW, Mitchell AD, Powers W, Applegate TJ (2006) Effect of dietary phosphorus, phytase, and 25-hydroxycholecalciferol on broiler chicken bone mineralization, litter phosphorus, and processing yields. J Poult Sci 85:1200–1211Google Scholar
  10. Angel R, Saylor WW, Dhandu AS, Powers W, Applegate TJ (2005) Effects of dietary phosphorus, phytase, and 25-hydroxycholecalciferol on performance of broiler chickens grown in floor pens. Poult Sci 84:1031–1044Google Scholar
  11. Angel R, Tamim NM, Applegate TJ, Dhandu AS, Ellestad LE (2002) Phytic acid chemistry: influence of phytin phosphorus availability and phytase efficacy. J Appl Poult Res 11:471–480Google Scholar
  12. Applegate T, Ange JR, Classen HL (2003) Effect of dietary calcium, 25-hydroxycholecalciferol, and bird strain on small intestinal phytase activity in broiler chickens. Poult Sci 82:1140–1148Google Scholar
  13. Applegate TJ, Angel CR, Classen HL, Newkirk RW, Maenz DD (2000) Effect of dietary calcium concentration and 25-hydroxycholecalceferol on phytate hydrolysis and intestinal phytase activity in broilers. Poult Sci 79(Suppl. 1):21 (Abstr.)Google Scholar
  14. Augspurger NR, Baker DH (2004) High dietary phytase levels maximize phytate-phosphorus utilization but do not affect protein utilization in chicks fed phosphorus- or amino acid-deficient diets. J Anim Sci 82:1100–1107Google Scholar
  15. Ballam GC, Nelson TS, Kirby LK (1985) Effect of different levels of calcium and phosphorus on phytate hydrolysis by chicks. Nutr Reports Int 32:909–913Google Scholar
  16. Blaabjerg K, Carlsson NG, Hansen MJ, Poulsen HD (2010) Effect of heat-treatment, phytase, xylanase and soaking time on inositol phosphate degradation in vitro in wheat, soybean meal and rapeseed cake. Anim Feed Sci Technol 162:123–134Google Scholar
  17. Boros D, Marquardt RR, Guenter W, Brufau J (2002) Chick adaptation to diets based on milling fractions of rye varying in arabinoxylans content. Anim Feed Sci Technol 101:135–149Google Scholar
  18. Brejnholt SM, Dionisio G, Glitsoe V, Skov LK, Brinch PH (2011) The degradation of phytate by microbial and wheat phytases is dependent on the phytate matrix and the phytase origin. J Sci Food Agric 91:1398–1405Google Scholar
  19. Burkholder JA, Glasgow HB (1997) Pfiesteria piscicidia and other Pfiesteria-dinoflagellates behaviors, impacts, and environmental controls. Limnol Oceanogr 42:1052–1075Google Scholar
  20. Butani JB, Parnerkar S (2015) Role of microbial phytase in broiler nutrition-a review. J Livestock Sci 6:113–118Google Scholar
  21. Camden BJ, Morel PCH, Thomas DV, Ravindran V, Bedford MR (2001) Effectiveness of exogenous microbial phytase in improving the bioavailabilities of phosphorus and other nutrients in maize-soya-bean meal diets for broilers. J Anim Sci 73:289–297Google Scholar
  22. Carre B, Idi A, Maisonnier S, Melcion JP, Oury FX, Gomez J, Pluchard P (2002) Relationship between digestibilities off ood components and characteristics of wheats (Triticum aestivum) introduced as the only cereal source in broiler chicken diet. Br Poult Sci 43:404–415Google Scholar
  23. Celi L, Barberis E (2005) Abiotic stabilization of organic phosphorus in the environment. In: Turner BL, Frossard E, Baldwin DS (eds) Organic phosphorus in the environment. CABI Publishing, WallingfordGoogle Scholar
  24. Chan KY, VanZwieten L, Meszaros L, Downie A, Joseph S (2008) Using poultry litter biochars as soil amendments. Aust J Soil Res 46:437–444Google Scholar
  25. Chung TK, Rutherfurd SM, Thomas DV, Moughan PJ (2013) Effect of two microbial phytases on mineral availability and retention and bone mineral density in low-phosphorus diets for broilers. Br Poult Sci 54(3):362–373Google Scholar
  26. Conte JA, Teixeira AS, Fialho ET (2003) Efeito da fitase e xilanasesobre o desempenho e as característicasósseas de frangos de cortealimentados com diet as contendofarelo de arroz. Rev Bras Zootec 32(5):1147–1156Google Scholar
  27. Cromwell GL, Coffey RD (1991) Phosphorus - a key essential nutrient, yet a possible major polluant - its central role in animal nutrition. In: Alltech’s Annual Symposium of Biotechnology in the Feed Industry, 7. Nicholasville. Proceedings Nicholasville: Alltech Technical Publications 133-145Google Scholar
  28. Dankowiakowska A, Kozlowska I, Bednarczyk M (2013) Probiotics, prebiotics and snybiotics in poultry-mode of action, limitation and achievements. J Cent Eur Agric 14:467–478Google Scholar
  29. Dozier W, Perryman K, Hess J (2015) Apparent ileal amino acid digestibility of reduced-oil distillers dried grains with soluble fed to broilers from 23 to 31 days of age. J Poult Sci 94:379–383Google Scholar
  30. Eckhout W, DePaepe M (1994) Total phosphorus, phytate phosphorus and phytase activity in plant feedstuffs. Anim Feed Sci Technol 47:19–29Google Scholar
  31. Emiola A, Woyengo TA, Owusu-Asiedu A, Guenter W, Simmins H, Nyachoti CM (2007) Performance and nutrient utilization in broilers fed corn-soybean meal-based diets supplemented with thermo-tolerant phytase. Poult Sci 86(Suppl.1):962 (Abstr.)Google Scholar
  32. FAO (2006) Food and agriculture organization of the United Nations. World agriculture: towards 2030/2050 interim report. FAOSTAT, RomeGoogle Scholar
  33. Garrett JB, Kretz KA, ODonoghue E, Kerovuo J, Kim W, Barton NR, Hazlewood GP, Short JM, Robertson DE, Gray KA (2004) Enhancing the thermal tolerance and gastric performance of a microbial phytase for use as a phosphate-mobilizing monogastric-feed supplement. Appl Environ Microbiol 70:3041–3046Google Scholar
  34. Greiner R, Haller E, Konietzny U, Jany KD (1997) Purification and characterization of a phytase from Klebsiellaterrigenda. Arch Biochem Biophys 341:201–206Google Scholar
  35. Hansen D, Nelson J, Binford G, Sims T, Saylor B (2005) Phosphorus in poultry litter: new guidelines from the University of Delaware. College of Agriculture and Natural Resources. University of Delaware, NewarkGoogle Scholar
  36. Haraldsson AK, Rimsten L, Alminger ML, Andersson R, Andlid T, Aman P, Sandberg AS (2004) Phytate content is reduced and b-glucanase activity suppressed in malted barley steeped with lactic acid at high temperature. J Sci Food Agric 84:653–662Google Scholar
  37. Harland FB, Morris ER (1995) Phytin: a good or a bad food component. Nutr Res 15:733–754Google Scholar
  38. Harmel RD, Smith DR, Haney RL, Dozier M (2009) Nitrogen and phosphorus runoff from cropland and pasture fields fertilized with poultry litter. J Soil Water Conserv 64:400–412Google Scholar
  39. Howarth RW (2008) Coastal nitrogen pollution: a review of sources and trends globally and regionally. Harmful Algae 8:14–20Google Scholar
  40. Howarth RW, Anderson DA, Church TM, Greening H, Hopkinson CS, Huber W, Marcus N, Naiman RJ, Segerson K, Sharpley AN, Wiseman WJ (2000) Clean coastal waters: understanding and reducing the effects of nutrient pollution. National Academy Press, National Research Council, Washington, DCGoogle Scholar
  41. Jacela JY, DeRouchey JM, Tokach MD, Goodband RD, Nelssen JL, Renter DG, Dritz SS (2010) Feed additives for swine: fact sheets-prebiotics and probiotics and phytogenics. J Swine Health Prod 18:87–91Google Scholar
  42. Jendza JA, Dilger RN, Sands JS, Adeola O (2006) Efficacy and equivalency of an Escherichia coli-derived phytase for replacing inorganic phosphorus in the diets of broiler chickens and young pigs. J Anim Sci 84:3364–3374Google Scholar
  43. Jeppeson E, Sondergaard M, Sondergaard M, Christofferson K (1998) The structuring role of submerged macrophytes in lakes. Springer, BerlinGoogle Scholar
  44. Jongbloed AW, Kemme PA (1990) Effect of pelleting mixed feeds on phytase activity and the apparent absorbability of phosphorus and calcium in pigs. Anim Feed Sci Technol 28:233–242Google Scholar
  45. Kaiser DE, Mallarino AP, Haq MU (2009) Runoff phosphorus loss immediately after poultry manure application as influenced by the application rate and tillage. J Environ Qual 38:299–308Google Scholar
  46. Kebreab E, Hansen AV, Strathe AB (2012) Animal production for efficient phosphate utilization: from optimized feed to high efficiency livestock. Curr Opin Biotechnol 23:872–877Google Scholar
  47. Kelleher BP, Leahy JJ, Henihan AM, Odwyer TF, Sutton D, Leahy MJ (2002) Advances in poultry litter disposal technology – a review. Bioresour Technol 83:27–36Google Scholar
  48. Kemme PA, Schlemmer U, Mroz Z, Jongbloed AW (2006) Monitoring the effect of microbial phytase on ileal phosphorus and amino acid Environ. Qual 34:1896–1909Google Scholar
  49. Kerr MJ, Classen HL, Newkirk RW (2000) The effects of gastrointestinal tract micro-flora and dietary phytase on inositol hexaphosphate hydrolysis in the chicken. J Poult Sci 79(Supp l.1):11Google Scholar
  50. Keshavarz K (2000) Nonphytate phosphorus requirement of laying hens with and without phytase on a phase feeding program. Poult Sci 79:748–763Google Scholar
  51. Kornegay ET (2001) Digestion of phosphorus and other nutrients: the role of phytases and factors influencing their activity. In: Bedford MR, Partridge GG (eds) Enzymesinfarm animal nutrition. Cab Publishing, Wallingford, p 432Google Scholar
  52. Kuhn I, Ralf G, Janos T (2012) The effect of phytase on ileal phosphorus digestibility and IP6degredation in broilers. NF Pc 290-2Google Scholar
  53. Lan GQ, Abdullah N, Jalaludin S, Ho YW (2002) Efficacy of supplementation of a phytase-producing bacterial culture on the performance and nutrient use of broiler chickens fed corn-soybean meal diets. Poult Sci 81(10):1522–1532Google Scholar
  54. Lalpanmawia H, Elangovan AV, Sridhar M, Shet D, Ajith S, Pal DT (2014) Efficacy of phytase on growth performance, nutrient utilization and bone mineralization in broiler chicken. Anim Feed Sci Technol 192:81–89Google Scholar
  55. Lei XG, KU PK, Miller ER, Yokoyama MT, Ullrey DE (1994) Calcium level affects the efficacy of supplemental microbial phytase in corn-soybean meal diets of weanling pigs. J Anim Sci 72:139–143Google Scholar
  56. Leytem AB, Willing BP, Thacker PA (2008) Phytate utilization and phosphorus excretion by broiler chickens fed diets containing cereal grains varying in phytate and phytase content. Anim Feed Sci Technol 146:160–168Google Scholar
  57. Liu N, Liu GH, Li FD, Sands JS, Zhang S, Zheng AJ, Ru YJ (2007) Efficacy of phytases on egg production and nutrient digestibility in layers fed reduced phosphorus diets. Poult Sci 86:2337–2342Google Scholar
  58. Ma Q, Tipping RH, Leforestier C (2008) Temperature dependences of mechanisms responsible for the water-vapor continuum absorption: 1. Far wings of allowed lines. J Chem Phys 128:124313Google Scholar
  59. Maenz DD, Classen HL (1998) Phytase activity in the small intestinal brush border membrane of the chicken. Poult Sci 77:557–563Google Scholar
  60. Maguire RO, Sims JT, Saylor WW, Turner BL, Angel R, Applegate TJ (2004) Influence of phytase addition to poultry diets on phosphorus forms and solubility in litters and amended soils. J Environ Qual 33:2306–2316Google Scholar
  61. Maison T, Liu Y, Stein HH (2015) Apparent and standardized total tract digestibility by growing pigs of phosphorus in canola meal from North America and 00-rapeseed meal and 00-rapeseed expellers from Europe without and with microbial phytase. J Anim Sci 93(7):3494–3502Google Scholar
  62. Manobhavan M, Elangovan AV, Sridhar M, Shet D, Ajith S, Pal DT, Gowda NK (2015) Effect of super dosing of phytase on growth performance, ileal digestibility and bone characteristics in broilers fed corn-soya-based diets. J Anim Physiol Anim Nutr 100:93–100Google Scholar
  63. Marounek M, Skrivan M, Dlouha G, Brenova N (2008) Availability of phytate phosphorus and endogenous phytase activity in the digestive tract of laying hens 20 and 47 weeks old. Anim Feed Sci Technol 146:353–359Google Scholar
  64. McGrath S, Maguire RO, Tacy BF, Kike JH (2009) Improving soil nutrition with poultry litter application in low input forage systems. Agron J 102:48–54Google Scholar
  65. McGrath JM, Sims JT, Maguire RO, Saylor WW, Angel R, Turner BL (2005) Broiler diet modification and litter storage: impacts on phosphorus in litters, soils, and runoff. J Environ Qual 34:1896–1909Google Scholar
  66. Millennium (2005) Ecosystem assessment. In: Synthesis report. Island, Washington, DC. www.MAweb.org Google Scholar
  67. Millner PD (2009) Bioaerosols associated with animal production systems. Bioresour Technol 100:5379–5385Google Scholar
  68. Mittal A, Singh G, Goyal V, Yadav A, Aneja KR, Gautam SK, Aggarwal NK (2011) Isolation and biochemical characterization of acido-thermophilic extracellular phytase producing bacterial strain for potential application in poultry feed. J Microbiol 4:273–282Google Scholar
  69. Mou CT (2016) The effects of various concentrations of phytase on broiler growth performance, phosphorus digestibility, tibia ash, and phosphorus utilization. Thesis of the faculty of the Virginia polytechnic institute and state university. Blacksburg, VirginiaGoogle Scholar
  70. Mullaney EJ, Ullah AHJ (2003) The term phytase comprises several different classes of enzymes. Biochem. Biophys. Res Commun 312:179–184Google Scholar
  71. Nahm KH (2002) Efficient feed nutrient utilization to reduce pollutants in poultry and swine manure. Crit Rev Environ Sci Technol 32:1–16Google Scholar
  72. Nutrient Requirement Council (NRC) (2007) 7th Revised. National academy press, Washington, DCGoogle Scholar
  73. National Research Council (NRC) (1994) Nutrient requirements of poultry. 9.ed. Washington, DC: National Academy of Science 155p.Google Scholar
  74. Nelson TS, Shieh TR, Wodzinski RJ, Ware JR (1971) Effect of supplemental phytase on utilization of phytate phosphorus by chicks. The J Nutr 101:1289–1293Google Scholar
  75. Oatway L, Vasanthan T, Helm JH (2001) Phytic acid. Food Rev Int 17:419–431Google Scholar
  76. Onyango EM, Bedford MR, Adeola O (2005) Phytase activity along the digestive tract of the broiler chick: a comparative study of an Escherichia coli-derived and Peniophoralycii phytase. Can J Anim Sci 85:61–68Google Scholar
  77. Patterson PH, Moore PA, Angel R (2005) Phosphorus and poultry nutrition In ‘Phosphorus: Agriculture and the environment’. (Eds JT Sims, AN Sharpley) 635-682Google Scholar
  78. Peter W (1992) Investigations on the use of phytase in the feeding of laying hens. Page 672 in : Proceedings XIX. Worlds Poultry Congress, AmsterdamGoogle Scholar
  79. Phillippy BQ (1999) Susceptibility of wheat and Aspergillus niger phytases to inactivation by gastrointestinal enzymes. J Agric Food Chem 47:1385–1388Google Scholar
  80. Powell S, Johnston S, Gaston L, Southern LL (2008) The effect of dietary phosphorus level and phytase supplementation on growth performance, bone-breaking strength, and litter phosphorus concentration in broilers. Poult Sci 87:949–957Google Scholar
  81. Rapp C, Lantzsch HJ, Drochner W (2001) Hydrolysis of phytic acid by intrinsic plant and supplemented microbial phytase (Aspergillus niger) in the stomach intestine ogmini pigs fitted with re-entrant cannulas: 3. Hydrolysis of phytic acid (IP6) and occurrence of products (IP5, IP4, IP3 and IP2). J Anim Physiol Anim Nutr (Berl) 85:420–430Google Scholar
  82. Ravindran V, Bryden WL, Kornegay ET (1995) Phytases: occurrence, bioavailability and implications in poultry nutrition. Poult Avian Biol Rev 6:125–143Google Scholar
  83. Ravindran V, Morel PC, Partridge H, Hruby GGM, Sands JS (2006) Influence of an Escherichia coli-derived phytase on nutrient utilization in broiler starters fed diets containing varying concentrations of phytic acid. Poult Sci 85:82–89Google Scholar
  84. Rutherfurd SM, Chung TK, Morel PCH, Moughan PJ (2004) Effect of microbial phytase on ileal digestibility of phytate phosphorus, total phosphorus, and amino acids in a low-phosphorus diet for broilers. Poult Sci 83:61–68Google Scholar
  85. Rutherfurd SM, Chung TK, Moughan PJ (2002) The effect of microbial phytase on ileal phosphorus and amino acid digestibility in the broiler chicken. Br Poult Sci 43(4):598–606Google Scholar
  86. Schiffman S, Williams M (2005) Science of odor as a potential health issue. J Environ Qual 34:129–138Google Scholar
  87. Schlemmer U, Jany KD, Berk A, Schulz E, Rechkemmer G (2001) Degradation of phytate in the gut of pigs-pathway of gastro-intestinal inositol-phosphate hydrolysis and enzymes involved. Arch Anim Nutr 55:255–280Google Scholar
  88. Selle PH, Cowieson AJ, Ravindran V (2009a) Consequences of calcium interactions with phytate and phytase for poultry and pigs. Livest Sci 124(1):126–141Google Scholar
  89. Selle PH, Ravindran V, Partridge GG (2009b) Beneficial effects of xylanase and/or phytase inclusions on ileal amino acid digestibility, energy utilisation, mineral retention and growth performance in wheat-based broiler diets. Anim Feed Sci Technol 153:303–313Google Scholar
  90. Selle PH, Ravindran V (2007) Microbial phytase in poultry nutrition. Anim Feed Sci Technol 135:1–41Google Scholar
  91. Sharpley AN, Herron S, Daniel T (2007) Overcoming the challenges of phosphorus-based management challenges in poultry farming. J Soil Water Conserv 58:30–38Google Scholar
  92. Silversides FG, Hruby M (2009) Feed formulation using phytase in laying hen diets. J Appl Poult Res 18:15–22Google Scholar
  93. Silversides FG, Scott TA, Korver DR, Afsharmanesh M, Hruby M (2006) A study on the interaction of xylanase and phytase enzymes in wheat-based diets fed to commercial phytase and xylanase alone or in combination. Anim Feed Sci Technol 146:113–123Google Scholar
  94. Silversides FG, Scott TA, Bedford MR (2004) The effect of phytase enzyme and level on nutrient extraction by broilers. Poult Sci 83:985–989Google Scholar
  95. Simon O, Igbasan F (2002) In vitro properties of phytases from various microbial origins. Int J Food Sci Technol 37:813–822Google Scholar
  96. Sims JT, Bergstrom L, Bowman BT, Oenema O (2005) Nutrient management for intensive animal agriculture: policies and practices for sustainability. Soil Use Manag 21:141–151Google Scholar
  97. Smulikowska S, Jan C, Anna M (2010) Effect of an organic acid blend and phytase added to a rapeseed cake-containing diet on performance, intestinal morphology, caecal microflora activity, and thyroid status of broiler chickens. J Anim Physiol Anim Nutr 94:15–23Google Scholar
  98. Sousa JPL, Albino LFT, Vaz RGMV, Rodrigues KF, DaSilva GF, Renno LN, Barross VRSM, Kaneko IN (2015) The effect of dietary phytase on broiler performance and digestive, bone, and blood biochemistry characteristics. Revista Brasileira de Ciencia Avícola 17:69–76Google Scholar
  99. Steiner T, Mosenthin R, Zimmermannb B, Greiner R, Roth S (2007) Distribution of phytase activity, total phosphorus and phytate phosphorus in legume seeds, cereals and cereal byproducts as influenced by harvest year and cultivar. Anim Feed Sci Technol 133:320–324Google Scholar
  100. Suttle NF (2010) Mineral nutrition of livestock: Fourth Edition. CABI, Wallingford, pp 1–547Google Scholar
  101. Szogi AA, Vanotti MB (2009) Prospects for phosphorus recovery from poultry litter. Bioresour Technol 100:5461–5465Google Scholar
  102. Tamim NM, Angel R, Christman M (2004) Influence of dietary calcium and phytase on phytate phosphorus hydrolysis in broiler chickens. Poult Sci 83(8):1358–1367Google Scholar
  103. Tamim NM, Angel R (2003) Phytate phosphorus hydrolysis as influenced by dietary calcium and micro-mineral source in broiler diets. J Agric Food Chem 51(16):4687–4693Google Scholar
  104. Toor GS, Hunger BE (2009) Phosphorus and trace metal dynamics in soils amended with poultry litter and granulates. Soil Use Manag 25:409–418Google Scholar
  105. USEPA (1996) Environmental indicators of water quality in the United States. EPA 841-R-96-002. USEPA, Office of Water (4503F), U.S. Government. Printing Office, Washington, DCGoogle Scholar
  106. Viveros A, Centeno C, Brenes A, Canales R, Lozano A (2000) Phytase and acid phosphatase activities in plant feedstuffs. J Agric Food Chem 48:4009–4013Google Scholar
  107. Walk C, Bedford M, Santos T, Paiva D, Bradley J, Wladecki H, Honaker C, McElroy A (2013) Extra-phosphoric effects of super doses of a novel microbial phytase. Poult Sci 92(3):719–725Google Scholar
  108. Weremko D, Fandrejeweski H, Zebrowska T (1997) Bioavailability of phosphorus in feeds of plant origin for pigs. Asian-Australasian J Anim Sci 10:551–566Google Scholar
  109. Wilson MA, Carpenter SR (1999) Economic valuation of freshwater ecosystem services in the United States: 1971–1997. Ecol Appl 9:772-783Google Scholar
  110. Woyengo TA, Nyachoti CM (2011) Review: Supplementation of phytase and and carbohydrates to diets for poultry. Can J Anim Sci 91:177–192Google Scholar
  111. Woyengo TA, Slominski BA, Jones RO (2010) Growth performance and nutrient utilization of broiler chickens fed diets supplemented with phytase alone or in combination with citric acid and multi carbohydrase. Poult Sci 89:2221–2229Google Scholar
  112. Wu P, Tian JC, Walker CE, Wang FC (2009) Determination of phytic acid in cereals – a brief review. Int J Food Sci Technol 44:1671–1676Google Scholar
  113. Wyss M, Brugger R, Kronenberger A, Remy R, Fimbel R (1999) Biochemical characterization of fungal phytases ( myo-inositol hexakisphosphate phosphohydrolases): catalytic properties. Appl Environ Microbiol 65:367–373Google Scholar
  114. Yu B, Jana YC, Chung TK, Lee TT, Chioua PWS (2004) Exogenous phytase activity in the gastrointestinal tract of broiler chickens. Anim Feed Sc Tech 117:295–303Google Scholar
  115. Zhang W, Aggrey SE, Pesti GM, Edwards HMJ, Bakalli RI (2003) Genetics of phytate phosphorus bioavailability: heritability and genetic correlation with growth and feed utilization traits in a random-bred chicken population. Poult Sci 82:1075–1079Google Scholar
  116. Zhang W, Aggrey SE, Pesti GM, Bakalli RI, Edwards HM (2005) Correlated responses to divergent selection for phytate phosphorus bioavailability in a random-bred chicken population. Poult Sci 84:536–542Google Scholar
  117. Zyla K, Gogol D, Koreleski J, Swiatkiewicz S, Ledoux DR (1999) Simultaneous application of phytase and xylanase to broiler feeds based on wheat: in vitro measurements of phosphorus and pentose release from wheats and wheat-based feeds. J Sci Food Agric 79:1832=1840Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Environmental Science and Engineering, School of Life Science and EngineeringSouthwest University of Science and TechnologyMianyangChina
  2. 2.Institute of ChemistryShah Abdul Latif UniversityKhairpurPakistan
  3. 3.Department of Animal Nutrition, Faculty of Animal Production and Technology, Cholistan University of Veterinary and Animal SciencesCUVASBahawalpurPakistan

Personalised recommendations