Advertisement

Biological Trace Element Research

, Volume 188, Issue 1, pp 35–44 | Cite as

Boron, Chromium, Manganese, and Nickel in Agricultural Animal Production

  • Jerry W. SpearsEmail author
Article
  • 78 Downloads

Abstract

This paper provides an overview of research that has been conducted with manganese (Mn), chromium (Cr), nickel (Ni), and boron (B) in poultry, swine, and ruminants. Manganese is an essential trace mineral that functions as an enzyme component and enzyme activator. A deficiency of Mn results in a variety of bone abnormalities, and Mn deficiency signs have been observed under practical conditions in poultry and cattle. Chromium can potentiate the action of insulin, but whether Cr is an essential trace mineral is controversial. Insulin sensitivity has been enhanced by Cr in cattle, swine, and broilers. Responses to Cr supplementation have been variable. Production responses to Cr supplementation have been most consistent in animals exposed to various stressors (heat, cold, weaning, etc). The legality of supplementing Cr to animal diets varies among countries, Cr sources, and animal species. A specific biochemical function for Ni and B has not been identified in mammals. Signs of Ni deficiency have been produced experimentally in a number of animal species. Nickel may affect rumen microbial fermentation in ruminants, as Ni is a component of bacterial urease and cofactor F430 in methanogenic bacteria. There is little evidence that dietary Ni limits animal production under practical conditions. Beneficial effects of B supplementation on growth and bone strength have been seen in poultry and swine, but results have been variable.

Keywords

Manganese Chromium Nickel Boron Poultry Cattle 

References

  1. 1.
    Underwood EJ, Mertz W (1987) Introduction. In: Mertz W (ed) Trace elements in human and animal nutrition, vol 1, 5th edn. Academic Press, Inc., San Diego, pp 1–19Google Scholar
  2. 2.
    Spears JW, Whisnant CS, Huntington GB, Lloyd KE, Fry RS, Krafka K, Lamptey A (2012) Chromium propionate enhances insulin sensitivity in growing cattle. J Dairy Sci 95:2037–2045Google Scholar
  3. 3.
    Vincent JB (2015) Is the pharmacological mode of action of chromium (III) as a second messenger? Biol Trace Elem Res 166:7–12Google Scholar
  4. 4.
    NRC (2005) Mineral tolerance of animals, 2nd edn. National Academies Press, WashingtonGoogle Scholar
  5. 5.
    Finley JM, Caton JS, Zhou Z, Davison KL (1997) A surgical model for determination of true absorption and biliary excretion of manganese in conscious swine fed commercial diets. J Nutr 127:2334–2341Google Scholar
  6. 6.
    Van Bruwaene R, Gerber GB, Kirchmann R, Colard J, Van Kerkom J (1984) Metabolism of 51Cr, 54Mn, 59Fe, and 60Co in lactating dairy cows. Health Phys 46:1069–1082Google Scholar
  7. 7.
    Halpin KM, Chausow DG, Baker DH (1986) Efficiency of manganese absorption in chicks fed corn-soy and casein diets. J Nutr 116:1747–1751Google Scholar
  8. 8.
    Hall ED, Symonds HW (1980) The maximum capacity of the bovine liver to excrete manganese in bile, and the effects of manganese load on the rate of excretion of copper, iron and zinc in bile. Br J Nutr 45:605–611Google Scholar
  9. 9.
    Erikson KM, Thompson KJ, Aschner M (2010) Transport and biological impact of manganese. In: Zalups RK, Koropatnick J (eds) Cellular and molecular biology of metals. CRC Press, New York, pp 127–141Google Scholar
  10. 10.
    Leach RM, Harris ED (1997) Manganese. In: O’Dell BL, Sunde RA (eds) Handbook of nutritionally essential mineral elements. Marcel Dekker, Inc., New York, pp 335–355Google Scholar
  11. 11.
    Suttle N (2010) Mineral nutrition of livestock, 4th edn. CABI, OxfordshireGoogle Scholar
  12. 12.
    Hidiroglou M, Ivan M, Bryan MK, Ribble CS, Janzen ED, Proulx JG, Elliot JI (1990) Assessment of the role of manganese in congenital joint laxity and dwarfism in calves. Ann Rech Vet 21:281–284Google Scholar
  13. 13.
    Valero G, Alley MR, Badcoe LM, Manktelow BW, Merrall M, Lewes GS (1990) Chondrodystrophy in calves associated with manganese deficiency. New Zealand Vet J 38:161–167Google Scholar
  14. 14.
    Staley GP, Van Der Lugt JJ, Axsel G, Loock AH (1994) Congenital skeletal malformations in Holstein calves associated with putative manganase deficiency. J South Afr Vet Ass 65:73–78Google Scholar
  15. 15.
    Lu L, Luo XG, Ji C, Liu B, Yu SX (2007) Effect of manganese supplementation and source on carcass traits, meat quality, and lipid oxidation in broilers. J Anim Sci 85:812–822Google Scholar
  16. 16.
    NRC (2016) Nutrient requirements of beef cattle, 8th edn. National Academies Press, WashingtonGoogle Scholar
  17. 17.
    NRC (2012) Nutrient requirements of swine, 11th edn. National Academies Press, WashingtonGoogle Scholar
  18. 18.
    Li S, Lin Y, Lu L, Xi L, Wang Z, Hao S, Zhang L, Li K, Luo X (2011) An estimation of the manganese requirement for broilers from 1 to 21 days of age. Biol Trace Elem Res 143:939–948Google Scholar
  19. 19.
    Ghost A, Mandal GP, Roy A, Patra AK (2016) Effects of supplementation of manganese with or without phytase on growth performance, carcass traits, muscle and tibia composition, and immunity in broiler chickens. Livestock Sci 191:80–85Google Scholar
  20. 20.
    Lu L, Ji C, Luo XG, Liu B, Yu SX (2006) The effect of supplemental manganese in broiler diets on abdominal fat deposition and meat quality. Anim Feed Sci Technol 129:49–59Google Scholar
  21. 21.
    Xiao JF, Zhang YN, Gu SG, Zhang HJ, Yue HY, Qi GH (2014) Manganese supplementation enhances the synthesis of glycosaminoglycan in eggshell membrane: a strategy to improve eggshell quality in laying hens. Poult Sci 93:380–388Google Scholar
  22. 22.
    Xiao JF, Wu SG, Zhang HJ, Yue HY, Wang J, Ji F, Qi GH (2015) Bioefficacy comparison of organic manganese with inorganic manganese for eggshell quality in Hy-Line brown laying hens. Poult Sci 94:1871–1878Google Scholar
  23. 23.
    Rheaume JA, Chavez TR (1989) Trace mineral metabolism in non-gravid, gestating and lactating gilts fed two dietary levels of manganese. J Trace Elem Electrolytes Health Dis 3:231–242Google Scholar
  24. 24.
    Legleiter LR, Spears JW, Lloyd KE (2005) Influence of dietary manganese on performance, lipid metabolism, and carcass composition of growing and finishing steers. J Anim Sci 83:2434–2439Google Scholar
  25. 25.
    Hansen SL, Spears JW, Lloyd KE, Whisnant CS (2006) Growth, reproductive performance, and manganese status of heifers fed varying concentrations of manganese. J Anim Sci 84:3375–3380Google Scholar
  26. 26.
    Hansen SL, Spears JW, Lloyd KE, Whisnant CS (2006) Feeding a low manganese diet to heifers during gestation impairs fetal growth and development. J Dairy Sci 89:4305–4311Google Scholar
  27. 27.
    Rojas MA, Dyer IA, Cassatt WA (1965) Manganese deficiency in the bovine. J Anim Sci 24:664–667Google Scholar
  28. 28.
    DiCostanzo A, Meiske JC, Plegge SD, Haggard DL, Chaloner KM (1986) Influence of manganese, copper and zinc on reproductive performance of beef cows. Nutr Rep Int 34:287–293Google Scholar
  29. 29.
    Masters DG, Paynter DI, Briegel J, Baker SK, Purser DB (1988) Influence of manganese intake on body, wool and testicular growth of young rams and on the concentration of manganese and the activity of manganese enzymes in tissues. Aust J Agric Res 39:517–524Google Scholar
  30. 30.
    Egan AR (1972) Reproductive responses to supplemental zinc and manganese in grazing Dorset Horn ewes. Aust J Exp Agric Anim Hus 12:131–135Google Scholar
  31. 31.
    Biehl RR, Baker DH, Deluca HF (1995) 1α-hydroxylated cholecalciferol compounds act additively with microbial phytase to improve phosphorus, zinc and manganese utilization in chicks fed soy-based diets. J Nutr 125:2407–2416Google Scholar
  32. 32.
    Mohanna C, Nys Y (1999) Changes in zinc and manganese availability in broiler chicks induced by vegetal and microbial phytase. Anim Feed Sci Technol 77:241–253Google Scholar
  33. 33.
    Attia YA, Qota EM, Bovera F, El-Din AE, Mansour SA (2010) Effect of amount and source of manganese and/or phytase supplementation on productive and reproductive performance and some physiological traits of dual purpose cross-bred hens in the topics. Br Poult Sci 51:235–245Google Scholar
  34. 34.
    Wedekind KJ, Baker DH (1990) Manganese utilization in chicks as affected by excess calcium and phosphorus ingestion. Poult Sci 69:977–984Google Scholar
  35. 35.
    Wedekind KJ, Titgemeyer EC, Twardock AR, Baker DH (1991) Phosphorus, but not calcium, affects manganese absorption and turnover in chicks. J Nutr 121:1776–1786Google Scholar
  36. 36.
    Bai S, Huang L, Luo Y, Wang L, Ding X, Wang J, Zeng Q, Zhang K (2014) Dietary manganese supplementation influences the expression of transporters involved in iron metabolism in chickens. Biol Trace Elem Res 160:352–360Google Scholar
  37. 37.
    Hansen SL, Trakooljul N, Liu HC, Moeser AJ, Spears JW (2009) Iron transporters are differentially regulated by dietary iron, and modifications are associated with changes in manganese metabolism in young pigs. J Nutr 139:1474–1479Google Scholar
  38. 38.
    Hansen SL, Ashwell MS, Moeser AJ, Fry RS, Knutson MD, Spears JW (2010) High dietary iron reduces transporters involved in iron and manganese metabolism and increases intestinal permeability in calves. J Dairy Sci 93:656–665Google Scholar
  39. 39.
    Woog-Valle J, Ammerman CB, Henry PR, Rao PV, Miles RD (1989) Bioavailability of manganese from feed grade manganese oxides for broiler chicks. Poult Sci 68:1368–1373Google Scholar
  40. 40.
    Henry PR, Ammerman CB, Littell RC (1992) Relative bioavailability of manganese from a manganese-methionine complex and inorganic sources for ruminants. J Dairy Sci 75:3473–3478Google Scholar
  41. 41.
    Smith MO, Sherman IL, Miller LC, Robbins KR (1995) Relative biological availability of manganese from manganese proteinate, manganese sulfate, and manganese monoxide in broilers reared at elevated temperatures. Poult Sci 74:702–707Google Scholar
  42. 42.
    Li SF, Luo XG, Lu L, Bu YQ, Liu B, Kuang X, Shao GZ, Yu SX (2005) Bioavailability of organic manganese sources in broilers fed high dietary calcium. Anim Feed Sci Technol 123-124:703–715Google Scholar
  43. 43.
    Brooks MA, Grimes JL, Lloyd KE, Valdez F, Spears JW (2012) Relative bioavailability in chicks of manganese from manganese propionate. J Appl Poult Res 21:126–130Google Scholar
  44. 44.
    Amoikon EK, Fernandez JM, Southern LL, Thompson DL, Ward TL, Olcott BM (1995) Effect of chromium tripicolinate on growth, glucose tolerance, insulin sensitivity, plasma metabolites, and growth hormone in pigs. J Anim Sci 73:1123–1130Google Scholar
  45. 45.
    Brooks MA, Grimes JL, Lloyd KE, Krafka K, Lamptey A, Spears JW (2016) Chromium propionate in broilers: effect on insulin sensitivity. Poult Sci 95:1096–1104Google Scholar
  46. 46.
    Spears JW, Lloyd KE, Krafka K (2017) Chromium concentrations in ruminant feed ingredients. J Dairy Sci 100:3584–3590Google Scholar
  47. 47.
    Scanes CG (2009) Perspectives on the endocrinology of poultry growth and metabolism. Gen Comp Endocrinol 163:24–32Google Scholar
  48. 48.
    Anderson RA (1994) Stress effects on chromium nutrition of humans and farm animals. In: Lyons TP, Jacques KA (eds) Biotechnology in the feed industry, proceedings of the Alltech 10th symposium. University Press, Nottingham, pp 267–274Google Scholar
  49. 49.
    Vincent JB (2017) New evidence against chromium as an essential trace element. J Nutr 147:2212–2019Google Scholar
  50. 50.
    Lloyd KE, Fellner V, McLeod SJ, Fry RS, Krafka K, Lamptey A, Spears JW (2010) Effects of supplementing dairy cows with chromium propionate on milk and tissue chromium concentrations. J Dairy Sci 93:4774–4780Google Scholar
  51. 51.
    Bunting LD, Fernandez JM, Thompson DL, Southern LL (1994) Influence of chromium picolinate on glucose usage and metabolic criteria in growing Holstein calves. J Anim Sci 72:1591–1599Google Scholar
  52. 52.
    Matthews JO, Southern LL, Fernandez JM, Pontif JE, Bidner TD, Odgaard RL (2001) Effect of chromium picolinate and chromium propionate on glucose and insulin kinetics of growing barrows and on growth and carcass traits of growing-finishing barrows. J Anim Sci 79:2172–2178Google Scholar
  53. 53.
    Evock-Clover CM, Polansky MM, Anderson RA, Steele NC (1993) Dietary chromium supplementation with or without somatotropin treatment alters serum hormones and metabolites in growing pigs without affecting growth performance. J Nutr 1123:1504–1512Google Scholar
  54. 54.
    Sano H, Nakai M, Kondo T, Terashima Y (1991) Insulin responsiveness to glucose and tissue responsiveness to insulin in lactating, pregnant, and nonpregnant, nonlactating beef cows. J Anim Sci 69:1122–1127Google Scholar
  55. 55.
    Stahlhut HS, Whisnant CS, Lloyd KE, Baird EJ, Legleiter LR, Hansen SL, Spears JW (2006) Effect of chromium supplementation and copper status on glucose and lipid metabolism in Angus and Simmental beef cows. Anim Feed Sci Technol 128:253–265Google Scholar
  56. 56.
    Hayirli A, Bremmer DR, Bertics SJ, Socha MT, Grummer RR (2001) Effect of chromium supplementation on production and metabolic parameters in periparturient dairy cows. J Dairy Sci 84:1218–1230Google Scholar
  57. 57.
    McNamara JP, Valdez F (2005) Adipose tissue metabolism and production responses to calcium propionate and chromium propionate. J Dairy Sci 88:2498–2507Google Scholar
  58. 58.
    Liu ZZ, Wu GQ, Zheng JX, An JY, Yang N, Xu GY (2010) Supplemental chromium picolinate promotes growth of broiler chickens by enhancing insulin receptor gene expression. J Anim Sci Biotech 1:7–14Google Scholar
  59. 59.
    Page TG, Southern LL, Ward TL, Thompson DL (1993) Effect of chromium picolinate on growth and serum and carcass traits of growing-finishing pigs. J Anim Sci 71:656–662Google Scholar
  60. 60.
    Lindemann MD, Wood CM, Harper AF, Kornegay ET, Anderson RA (1995) Dietary chromium picolinate additions improve gain:feed and carcass characteristics in growing-finishing pigs and increase litter size in reproducing sows. J Anim Sci 73:457–465Google Scholar
  61. 61.
    Jackson AR, Powell S, Johnston SL, Matthews JO, Bidner TD, Valdez FR, Southern LL (2009) The effect of chromium as chromium propionate on growth performance, carcass traits, meat quality, and the fatty acid profile of fat from pigs fed no supplemental dietary fat, choice white grease, or tallow. J Anim Sci 87:4032–4041Google Scholar
  62. 62.
    Mooney KW, Cromwell GL (1997) Effect of chromium picolinate and chromium chloride as potential carcass modifiers in swine. J Anim Sci 75:2661–2671Google Scholar
  63. 63.
    Matthews JO, Guzik AC, LeMieux FM, Southern LL, Bidner TD (2006) Effects of chromium propionate on growth, carcass traits, and pork quality of growing-finishing pigs. J Anim Sci 84:858–862Google Scholar
  64. 64.
    Lindemann MD, Carter SD, Chiba LI, Dove CR, LeMieux FM, Southen LL (2004) A regional evaluation of chromium tripicolinate supplementation of diets fed to reproducing sows. J Anim Sci 82:2972–2977Google Scholar
  65. 65.
    Wang L, Shi A, Jia Z, Su B, Shi B, Shan A (2013) The effects of dietary supplementation with chromium picolinate throughout gestation on productive performance, Cr concentration, serum parameters, and colostrum composition in sows. Biol Trace Elem Res 154:55–61Google Scholar
  66. 66.
    Jackson AR, Powell S, Johnston S, Shelton JL, Bidner TD, Valdez FR, Southern LL (2008) The effect of chromium propionate on growth performance and carcass traits in broilers. J Appl Poult Res 17:476–481Google Scholar
  67. 67.
    Zheng C, Huang Y, Xiao F, Lin X, Lloyd K (2016) Effects of supplemental chromium source and concentration on growth, carcass characteristics, and serum lipid parameters of broilers reared under normal conditions. Biol Trace Elem Res 169:352–358Google Scholar
  68. 68.
    Sahin N, Hayirli A, Orhan C, Tuzcu M, Akdemir F, Komorowski JR, Sahin K (2017) Effects of the supplemental chromium form on performance and oxidative stress in broilers exposed to heat stress. Poult Sci 96:4317–4324Google Scholar
  69. 69.
    Kegley EB, Spears JW, Brown TT (1996) Immune response and disease resistance of calves fed chromium nicotinic acid complex or chromium chloride. J Dairy Sci 79:1278–1283Google Scholar
  70. 70.
    Rajalekshmi M, Sugumar C, Chirakkal H, Ramarao SV (2014) Influence of chromium propionate on the carcass characteristics and immune response of commercial broiler birds under normal rearing conditions. Poult Sci 93:574–580Google Scholar
  71. 71.
    Smith KL, Waldron MR, Drackley JK, Socha MT, Overton TR (2005) Performance of dairy cows as affected by prepartum dietary carbohydrate source and supplementation with chromium through the transition period. J Dairy Sci 88:255–263Google Scholar
  72. 72.
    Krafilzadeh F, Karami shabankarch H, Targhibi MR (2012) Effect of chromium supplementation on productive and reproductive performances and some metabolic parameters in late gestation and early lactation of dairy cows. Biol Trace Elem Res 149:42–49Google Scholar
  73. 73.
    Rockwell RJ, Allen MS (2016) Chromium propionate supplementation during the peripartum period interacts with starch source fed postpartum: production responses during the immediate postpartum and carryover periods. J Dairy Sci 99:4453–4463Google Scholar
  74. 74.
    Vargas-Rodriguez CF, Yuan K, Titgemeyer EC, Mamedova LK, Griswold KE, Bradford BJ (2014) Effects of supplemental chromium propionate and rumen-protected amino acids on productivity, diet digestibility, and energy balance of peak-lactation dairy cows. J Dairy Sci 97:3815–3821Google Scholar
  75. 75.
    Aragon VEF, Graca DS, Norte AL (2001) Supplemental high chromium yeast and reproductive performance of grazing primiparous Zebu cows. Arg Bras Med Vet Zoo 53:624–628Google Scholar
  76. 76.
    Stahlhut HS, Whisnant CS, Spears JW (2006) Effect of chromium supplementation and copper status on performance and reproduction of beef cows. Anim Feed Sci Technol 128:266–275Google Scholar
  77. 77.
    Sands JS, Smith MO (1999) Broilers in heat stress conditions: effects of dietary manganese proteinate or chromium picolinate supplementation. J Appl Poult Res 8:290–287Google Scholar
  78. 78.
    Sahin K, Sahin N, Onderci M, Gursu F, Cikim G (2002) Optimal dietary concentration of chromium for alleviating the effect of heat stress on growth, carcass qualities, and some serum metabolites of broiler chickens. Biol Trace Elem Res 89:53–64Google Scholar
  79. 79.
    Huang Y, Yang J, Xiao F, Lloyd K, Lin X (2016) Effects of supplemental chromium source and concentration on growth performance, carcass traits, and meat quality of broilers under heat stress conditions. Biol Trace Elem Res 170:216–223Google Scholar
  80. 80.
    Samanta S, Haldar S, Bahadur V, Ghosh TK (2008) Chromium picolinate can ameliorate the negative effects of heat stress and enhance performance, carcass and meat traits in broiler chickens by reducing the circulatory cortisol level. J Sci Food Agric 88:787–796Google Scholar
  81. 81.
    Toghyani M, Toghyani M, Shivazad M, Gheisari A, Bahadoran R (2012) Chromium supplementation can alleviate the negative effects of heat stress on growth performance, carcass traits, and meat lipid oxidation of broiler chicks without any adverse impacts on blood constituents. Biol Trace Elem Res 146:171–180Google Scholar
  82. 82.
    Sahin K, Kucuk O, Sahin N (2001) Effects of dietary chromium picolinate supplementation on performance and plasma concentrations of insulin and corticosterone in laying hens under low ambient temperature. J Anim Physiol Anim Nutr 85:142–147Google Scholar
  83. 83.
    Jahanian R, Rasouli E (2015) Dietary chromium methionine supplementation could alleviate immunosuppressive effects of heat stress in broiler chicks. J Anim Sci 93:3355–3363Google Scholar
  84. 84.
    Liu F, Cottrell JJ, Wijesiriwardana U, Kelly FW, Chauhan SS, Pustovit RV, Gonzales-Rivas PA, DiGiacomo K, Leury BJ, Celi P, Dunshea FR (2017) Effects of chromium supplementation on physiology, feed intake, and insulin related metabolism in growing pigs subjected to heat stress. Transl Anim Sci 1:116–125Google Scholar
  85. 85.
    Kim BG, Lindemann MD, Cromwell GL (2009) The effects of dietary chromium (III) picolinate on growth performance, blood measurements, and respiratory rate in pigs kept in high and low ambient temperature. J Anim Sci 87:1695–1704Google Scholar
  86. 86.
    Al-Saiady MY, Al-Shaikh MA, Al-Mufarrej SI, Al-Showeimi TA, Mogawer HH, Dirrar A (2004) Effect of chelated chromium supplementation on lactation performance and blood parameters of Holstein cows under heat stress. Anim Feed Sci Technol 117:223–233Google Scholar
  87. 87.
    Soltan MA (2010) Effect of dietary chromium supplementation on productive and reproductive performance of early lactating dairy cows under heat stress. J Anim Physiol Anim Nutr 94:264–272Google Scholar
  88. 88.
    Nikkhah A, Mirzaei M, Khorvash M, Rahmani HR, Ghorbani GR (2011) Chromium improves production and alters metabolism of early lactation cows in summer. J Anim Physiol Anim Nutr 95:81–89Google Scholar
  89. 89.
    Spears JW (2000) Micronutrients and immune function in cattle. Proc Nutr Soc 59:587–594Google Scholar
  90. 90.
    Bernhard BC, Burdick NC, Rounds W, Rathmann RJ, Carroll JA, Finck DN, Jennings MA, Young TR, Johnson BJ (2012) Chromium supplementation alters the performance and health of feedlot cattle during the receiving period and enhances their metabolic response to a lipopolysaccharide challenge. J Anim Sci 90:3879–3888Google Scholar
  91. 91.
    Spears JW (1984) Nickel as a “newer trace mineral” in the nutrition of domestic animals. J Anim Sci 59:823–835Google Scholar
  92. 92.
    Nielson FH, Myron DR, Givand SH, Ollerich DA (1975) Nickel deficiency and nickel-rhodium interaction in chicks. J Nutr 105:1607–1619Google Scholar
  93. 93.
    Hausinger RP (1987) Nickel utilization by microorganisms. Microbiol Rev 51:22–42Google Scholar
  94. 94.
    Eskew DL, Welch RM, Cary EE (1983) Nickel: an essential micronutrient for legumes and possibly all higher plants. Science 222:621–623Google Scholar
  95. 95.
    Spears JW, Smith CJ, Hatfield EE (1977) Rumen bacterial urease requirement for nickel. J Dairy Sci 60:1073–1076Google Scholar
  96. 96.
    Spears JW, Hatfield EE, Forbes RM (1979) Nickel for ruminants II. Influence of dietary nickel on performance and metabolic parameters. J Anim Sci 48:649–657Google Scholar
  97. 97.
    Starnes SR, Spears JW, Harvey RW (1984) Interaction between nickel and protein source in the ruminant. Biol Trace Elem Res 6:403–413Google Scholar
  98. 98.
    Oscar TP, Spears JW, Shih JCH (1987) Performance, methanogenesis and nitrogen metabolism of finishing steers fed monensin and nickel. J Anim Sci 64:887–896Google Scholar
  99. 99.
    Oscar TP, Spears JW (1988) Nickel-induced alterations of in vitro and in vivo ruminal fermentation. J Anim Sci 66:2313–2324Google Scholar
  100. 100.
    Cheng KJ, Wallace RJ (1979) The mechanism of passage of endogenous urea through the rumen wall and the role of ureolytic epithelial bacteria in the urea flux. Br J Nutr 42:553Google Scholar
  101. 101.
    Spears JW, Harvey RW, Samsell LJ (1986) Effects of dietary nickel and protein on growth, nitrogen metabolism and tissue concentrations of nickel, iron, zinc, manganese and copper in calves. J Nutr 116:1873–1882Google Scholar
  102. 102.
    Milne JS, Whitelaw FG, Price J, Shand WJ (1990) The effect of supplemental nickel on urea metabolism in sheep given a low protein diet. Anim Prod 50:507–512Google Scholar
  103. 103.
    Oscar TP, Spears JW (1990) Incorporation of nickel into ruminal factor F430 as affected by monensin and formate. J Anim Sci 68:1400–1404Google Scholar
  104. 104.
    Oscar TP, Mitchell DM, Engster HM, Malone BR, Watson WM (1995) Growth performance, carcass composition, and pigmentation of broiler fed supplemental nickel. Poult Sci 74:976–982Google Scholar
  105. 105.
    Spears JW, Jones EE, Samsell LF, Armstrong WD (1984) Effect of dietary nickel on growth, urease activity, blood parameters and tissue mineral concentrations in the neonatal pig. J Nutr 114:845–853Google Scholar
  106. 106.
    European Food Safety Authority (2015) Scientific opinion on the risks to animal and public health and the environment related to the presence of nickel in feed. EFSA J 13:4074Google Scholar
  107. 107.
    Nielsen FH (1997) Boron in human and animal nutrition. Plant Soil 193:199–208Google Scholar
  108. 108.
    Park M, Li Q, Shcheynikov N, Zeng W, Muallem S (2004) NaBCl is a ubiquitous electrogenic Na+-coupled borate transporter essential for cellular boron homeostasis and cell growth and proliferation. Mol Cell 16:331–341Google Scholar
  109. 109.
    Liao SF, Monegue JS, Lindermann MD, Cromwell GL, Matthews JC (2011) Dietary supplementation of boron differentially alters expression of borate transporter (NaBCl) mRNA by jejunum and kidney of pigs. Biol Trace Elem Res 143:901–912Google Scholar
  110. 110.
    Bozkurt M, Kucukyilmaz K (2015) An evaluation on the potential role of boron in poultry nutrition. Part I: production performance. World's Poult Sci J 71:327–338Google Scholar
  111. 111.
    Bozkurt M, Kucukyilmaz K (2015) The role of boron in poultry nutrition. Part II: compositional and mechanical properties of bone and egg quality. World Poult Sci J 71:483–492Google Scholar
  112. 112.
    Rossi AF, Miles RD, Damron BL, Flunker LK (1993) Effects of dietary boron supplementation on broilers. Poult Sci 72:2124–2130Google Scholar
  113. 113.
    Rossi AF, Butcher GD, Miles RD (1994) The interaction of boron with calcium, phosphorus and cholecalciferol in broilers. J Appl Anim Res 6:151–160Google Scholar
  114. 114.
    Wilson JH, Roszler PL (1997) Effects of boron on growing pullets. Biol Trace Elem Res 56:287–294Google Scholar
  115. 115.
    Qin X, Klandorf H (1991) Effect of dietary boron supplementation on egg production, shell quality, and calcium metabolism in aged broiler breeder hens. Poult Sci 70:2131–2138Google Scholar
  116. 116.
    Armstrong TA, Spears JW, Crenshaw TD, Nielsen FH (2000) Boron supplementation of a semipurified diet for weanling pigs improves feed efficiency and bone strength characteristics and alters plasma lipid metabolites. J Nutr 139:2575–2581Google Scholar
  117. 117.
    Hunt CD (2007) Dietary boron: evidence for essentiality and homeostatic control in humans and animals. In: Xu T, Goldbach HE, Brown PH, Bell RW, Fujiwara T, Hunt CD, Goldberg S, Shi L (eds) Advances in plant and animal boron nutrition. Springer, The Netherlands, pp 251–267Google Scholar
  118. 118.
    Armstrong TA, Spears JW (2001) Effect of dietary boron on growth performance, calcium and phosphorus metabolism, and bone mechanical properties in growing barrows. J Anim Sci 79:3120–3127Google Scholar
  119. 119.
    Armstrong TA, Spears JW, Lloyd KE (2001) Inflammatory response, growth, and thyroid hormone concentrations are affected by long-term boron supplementation in gilts. J Anim Sci 79:1549–1556Google Scholar
  120. 120.
    Armstrong TA, Flowers WL, Spears JW, Nielsen FH (2002) Long-term effects of boron supplementation on reproductive characteristics and bone mechanical properties in gilts. J Anim Sci 80:154–161Google Scholar
  121. 121.
    Armstrong TA, Spears JW (2003) Effect of boron supplementation of pig diets on the production of tumor necrosis factor-α and interferon-γ. J Anim Sci 81:2552–2561Google Scholar
  122. 122.
    Basoglu A, Sevinc M, Birdane FM, Boydak M (2002) Efficacy of sodium borate in the prevention of fatty liver in dairy cows. J Vet Intern Med 16:732–735Google Scholar
  123. 123.
    Basoglu A, Baspinar N, Tenori L, Vignoli A, Gulersoy E (2017) Effects of boron supplementation on peripartum dairy cows’ health. Biol Trace Elem Res 179:218–225Google Scholar
  124. 124.
    Bhasker TV, Gowda NKS, Pal DT, Bhat SK, Krishnamoorthy P, Mondal S, Pattanaik AK, Verma AK (2017) Influence of boron supplementation on performance, immunity and antioxidant status of lambs fed diets with or without adequate level of calcium. PLoS One 12:e0187203Google Scholar
  125. 125.
    Fry RS, Lloyd KE, Jacobi SK, Siciliano PD, Robarge WP, Spears JW (2010) Effect of dietary boron on immune function in growing beef steers. J Anim Physiol Anim Nutr 94:273–279Google Scholar
  126. 126.
    Fry RS, Brown TT, Lloyd KE, Hansen SL, Legleiter LR, Robarge WP, Spears JW (2011) Effect of dietary boron on physiological responses in growing steers inoculated with bovine herpesvirus type-1. Res Vet Sci 90:78–83Google Scholar
  127. 127.
    Brown TF, McCormick ME, Morris DR, Zeringue LK (1989) Effects of dietary boron on mineral balance in sheep. Nutr Res 9:503–512Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Animal ScienceNorth Carolina State UniversityRaleighUSA

Personalised recommendations