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http://dx.doi.org/10.5713/ajas.19.0945

Importance of micronutrients in bone health of monogastric animals and techniques to improve the bioavailability of micronutrient supplements - A review  

Upadhaya, Santi Devi (Department of Animal Resource and Science, Dankook University)
Kim, In Ho (Department of Animal Resource and Science, Dankook University)
Publication Information
Asian-Australasian Journal of Animal Sciences / v.33, no.12, 2020 , pp. 1885-1895 More about this Journal
Abstract
Vitamins and minerals categorized as micronutrients are the essential components of animal feed for maintaining health and improving immunity. Micronutrients are important bioactive molecules and cofactors of enzymes as well. Besides being cofactors for enzymes, some vitamins such as the fat-soluble vitamins, vitamin A and D have been shown to exhibit hormone-like functions. Although they are required in small amount, they play an influential role in the proper functioning of a number of enzymes which are involved in many metabolic, biochemical and physiological processes that contribute to growth, production and health. Micronutrients can potentially have a positive impact on bone health, preventing bone loss and fractures, decreasing bone resorption and increasing bone formation. Thus, micronutrients must be provided to livestock in optimal concentrations and according to requirements that change during the rapid growth and development of the animal and the production cycle. The supply of nutrients to the animal body not only depends on the amount of the nutrient in a food, but also on its bioavailability. The bioavailability of these micronutrients is affected by several factors. Therefore, several technologies such as nanoparticle, encapsulation, and chelation have been developed to improve the bioavailability of micronutrients associated with bone health. The intention of this review is to provide an updated overview of the importance of micronutrients on bone health and methods applied to improve their bioavailability.
Keywords
Bone Health; Bioavailability; Micronutrient; Minerals; Vitamins;
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1 Weiser H, Schlachter M, Probst HP, Flachowsky G, Schone F. Importance of vitamin D3, C and B6 for bone metabolism. Friedrich Schiller Universitat Jena Germany. Vitamins and other additives in humans and animals. 3rd Symposium 1991; Jena, Germany. p. 26-7.
2 Dikicioglu T, Yigit AA, Ozdemir, E. The effects of niacin on egg production and egg quality. Lalahan Hay Arast Enst Derg 2000;40:65-74.
3 Liu A, Feng L. Effects of supplementation of folic acid, ascorbic acid and cyanocobalamin on the performance of layers. Ningxia J Agro-For Sci Technol 1992;6:40-2.
4 Veum TL. Feed supplements: crystalline vitamins. In: Pond W, Ullrey D, Baer C, editors. Encyclopedia of animal science. 2nd Ed. Boca Raton, FL, USA: Taylor and Francis; 2011.
5 Mc Dowell LR. Vitamins in animal and human nutrition. 2nd Ed. Ames, IA, USA: Iowa State University Press; 2000.
6 Radwinska J, Zarczynska K. Effects of mineral deficiency on the health of young ruminants. J Elem 2014;19:915-28.
7 Wu D, Lewis ED, Pae M, Meydani SN. Nutritional modulation of immune function: analysis of evidence, mechanisms, and clinical relevance. Front Immunol 2019;9:3160. https://doi.org/10.3389/fimmu.2018.03160   DOI
8 DeLuca HF. Vitamin D: the vitamin and the hormone. Fed Proc 1974;33:2211-9.
9 Office of the Surgeon General (US). Bone health and osteoporosis: a report of the surgeon general. Rockville MD, USA: Office of the Surgeon General (US); 2004.
10 Garcia LA, King KK, Ferrini MG, Norris KC, Artaza JN. $1,25(OH)_{2}$ vitamin D3 stimulates myogenic differentiation by inhibiting cell proliferation and modulating the expression of promyogenic growth factors and myostatin in $C_{2}C_{12}$ skeletal muscle cells. Endocrinology 2011;152:2976-86. https://doi.org/10.1210/en.2011-0159   DOI
11 Dodds RA, Catterall A, Bitensky L, Chayen J. Abnormalities in fracture healing induced by vitamin B6-deficiency in rats. Bone 1986;7:489-95. https://doi.org/10.1016/8756-3282(86)90008-6   DOI
12 Masse PG, Pritzker KP, Mendes MG, Boskey AL, Weiser H. Vitamin B6 deficiency experimentally-induced bone and joint disorder: Microscopic, radiographic and biochemical evidence. Br J Nutr 1994;71:919-32. https://doi.org/10.1079/bjn19940196   DOI
13 Herrmann M, Wildemann, B, Wagner A, et al. Experimental folate and vitamin B12 deficiency does not alter bone quality in rats. J Bone Miner Res 2009;24:589-96. https://doi.org/10.1359/jbmr.081211   DOI
14 Holstein JH, Herrmann M, Schmalenbach J, et al. Deficiencies of folate and vitamin B12 do not affect fracture healing in mice. Bone 2010;47:151-5. https://doi.org/10.1016/j.bone.2010.04.592   DOI
15 Neve A, Corrado A, Cantatore FP. Osteocalcin: skeletal and extra-skeletal effects. J Cell Physiol 2013;228:1149-53. https://doi.org/10.1002/jcp.24278   DOI
16 Saura-Calixto F, Serrano J, Goni I. Intake and bioaccessibility of total polyphenols in a whole diet. Food Chem 2007;101: 492-501. https://doi.org/10.1016/j.foodchem.2006.02.006   DOI
17 Cancela L, Hsieh CL, Francke U, Price PA. Molecular structure, chromosome assignment, and promoter organization of the human matrix Gla protein gene. J Biol Chem 1990;265:15040-8.   DOI
18 Lombardi G, Perego S, Luzi L, Banfi G. A four-season molecule: osteocalcin. Updates in its physiological roles. Endocrine 2015;48:394-404. https://doi.org/10.1007/s12020-014-0401-0   DOI
19 Akbari S, Rasouli-Ghahroudi AA. Vitamin K and bone metabolism: A review of the latest evidence in preclinical studies. Biomed Res Int 2018;2018:4629383. https://doi.org/10.1155/2018/4629383   DOI
20 Schonfeldt HC, Pretorius B, Hall N. Bioavailability of nutrients. In: Caballero B, Finglas PM, Toldra F, editors. Encyclopedia of food and health. Oxford, UK: Academic Press; 2016. pp. 401-6. https://doi.org/10.1016/B978-0-12-384947-2.00068-4
21 Gropper SS, Smith JL. The digestive system: mechanism for nourishing the body. In: Gropper SS, Smith JL, Groff JL, editors. Advanced nutrition and human metabolism. 5th ed. Belmont, CA, USA: Wadsworth, Cengage Learning; 2009. pp. 33-62.
22 Ma YL, Lindemann MD, Webb SF, Rentfrow G. Evaluation of trace mineral source and preharvest deletion of trace minerals from finishing diets on tissue mineral status in pigs. Asian-Australas J Anim Sci 2018;31:252-62. https://doi.org/10.5713/ajas.17.0189   DOI
23 Li KX, Wang JS, Yuan D, Zhao RX, Wang YX, Zhan XA. Effects of different selenium sources and levels on antioxidant status in broiler breeders. Asian-Australas J Anim Sci 2018;31:1939-45. https://doi.org/10.5713/ajas.18.0226   DOI
24 Singh OV. Bio-nanoparticles: biosynthesis and sustainable biotechnological implications. Hoboken, NJ, USA: Wiley-Blackwell; 2015.
25 Hill CH, Matrone G. Chemical parameters in the study of in vivo and in vitro interactions of transition elements. Fed Proc 1970;29:1474-81.
26 Hambridge KM. Micronutrient bioavailability: Dietary reference intakes and a future perspective. Am J Clin Nutr 2010; 91:1430S-2S. https://doi.org/10.3945/ajcn.2010.28674B   DOI
27 Truswell AS. Vitamin B12. Nutr Diet 2007;64(Suppl 4):S120-5. https://doi.org/10.1111/j.1747-0080.2007.00198.x   DOI
28 Shukla A, Iravani S. Green synthesis, characterization and applications of nanoparticles. Amsterdam, The Netherlands: Elsevier; 2018.
29 Oehlke K, Adamiuk M, Behsnilian D, et al. Potential bioavailability enhancement of bioactive compounds using food-grade engineered nanomaterials: a review of the existing evidence. Food Funct 2014;5:1341-59. https://doi.org/10.1039/c3fo60067j   DOI
30 Jampliek J, Kos J, Kralova K. Potential of nanomaterial applications in dietary supplements and foods for special medical purposes. Nanomaterials 2019;9:296. https://doi.org/10.3390/nano9020296   DOI
31 Xia T, Lai W, Han M, Han M, Ma X, Zhang L. Dietary ZnO nanoparticles alter intestinal microbiota and inflammation response in weaned piglets. Oncotarget 2017;8:64878-91. https://doi.org/10.18632/oncotarget.17612   DOI
32 Joye IJ, Davidov-Pardo G, McClements DJ. Nanotechnology for increased micronutrient bioavailability. Trends Food Sci Technol 2014;40:168-82. https://doi.org/10.1016/j.tifs.2014.08.006   DOI
33 Ozturk B. Nanoemulsions for food fortification with lipophilic vitamins: production challenges, stability, and bioavailability. Eur J Lipid Sci Technol 2017;119:1500539. https://doi.org/10.1002/ejlt.201500539   DOI
34 Debski B. Supplementation of pigs diet with zinc and copper as alternative to conventional antimicrobials. Pol J Vet Sci 2016;19:917-24. https://doi.org/10.1515/pjvs-2016-0113   DOI
35 Upadhaya SD, YM Kim, KY Lee, IH Kim. Use of protected zinc oxide in lower doses in weaned pigs in substitution for the conventional high dose zinc oxide. Anim Feed Sci Technol 2018;240:1-10. https://doi.org/10.1016/j.anifeedsci.2018.03.012   DOI
36 Jiao Y, Li X, Kim IH. Changes in growth performance, nutrient digestibility, immune blood profiles, fecal microbial and fecal gas emission of growing pigs in response to zinc aspartic acid chelate. Asian-Australas J Anim Sci 2020;33:597-604. https://doi.org/10.5713/ajas.19.0057   DOI
37 Baker DH. Bioavailability of minerals and vitamins. In: Lewis AJ, Southern LL, editors. Swine nutrition. Boca Raton, FL, USA: CRC Press; 2001. pp. 357-79.
38 Baker DH. Cupric oxide should not be used as a copper supplement for either animals or humans. J Nutr 1999;129:2278-79. https://doi.org/10.1093/jn/129.12.2278   DOI
39 Ashmead HD, Graff DJ, Ashmead HH. Intestinal absorption of metal ions and chelates. Springfield, IL, USA: Thomas CC; 1985. pp. 118-25.
40 Mahdavi-Roshan M, Ebrahimi M, Ebrahimi A. Copper, magnesium, zinc and calcium status in osteopenic and osteoporotic post-menopausal women. Clin Cases Miner Bone Metab 2015; 12:18-21. https://doi.org/10.11138/ccmbm/2015.12.1.018   DOI
41 Wilson JH, Ruszler PL. Long term effects of boron on layer bone strength and production parameters. Br Poult Sci 1998; 39:11-5. https://doi.org/10.1080/00071669889312   DOI
42 Incharoen T, Tartrakoon W, Nakhon S, Treetan S. Effects of dietary silicon derived from rice hull ash on the meat quality and bone breaking strength of broiler chickens. Asian J Anim Vet Adv 2016;11:417-22. https://doi.org/10.3923/ajava.2016.417.422   DOI
43 Reffitt DM, Ogston N, Jugdaohsingh R, et al. Orthosilicic acid stimulates collagen type 1 synthesis and osteoblastic differentiation in human osteoblast-like cells in vitro. Bone 2003;32: 127-35. https://doi.org/10.1016/S8756-3282(02)00950-X   DOI
44 Jugdaohsingh R. Silicon and bone health. J Nutr Health Aging 2007;11:99-110.
45 Chapin RE, Ku WW, Kenney MA, McCoy H. The effects of dietary boric acid on bone strength in rats. Biol Trace Elem Res 1998;66:395-9. https://doi.org/10.1007/BF02783150   DOI
46 Boguszewska-Czubara A, Pasternak K. Silicon in medicine and therapy. J Elem 2011;16:489-97. https://doi.org/10.5601/jelem.2011.16.3.13
47 Norman AW. The vitamin D endocrine system. Physiologist 1985;28:219-32.
48 Holick MF. Sunlight, ultra violet radiation, vitamin D, and skin cancer: how much sunlight do we need? In: Reichrath J. editor. Sunlight, vitamin D and skin cancer. New York, USA: Springer-Verlag; 2014. pp. 1-16. https://doi.org/10.1007/978-1-4939-0437-2
49 Cashman KD, Seamans KM, Lucey AJ, et al. Relative effectiveness of oral 25-hydroxyvitamin D3 and vitamin D3 in raising wintertime serum 25-hydroxyvitamin D in older adults. Am J Clin Nutr 2012;95:1350-6. https://doi.org/10.3945/ajcn.111.031427   DOI
50 Driver JP, Pesti GM, Bakalli RI, Edwards HM, Jr. Calcium requirements of the modern broiler chicken as influenced by dietary protein and age. Poult Sci 2005;84:1629-39. https://doi.org/10.1093/ps/84.10.1629   DOI
51 Holick MF. Vitamin D: evolutionary, physiological and health perspectives. Curr Drug Targets 2011;12:4-18. https://doi.org/10.2174/138945011793591635   DOI
52 Razzaque MS. The dualistic role of vitamin D in vascular calcifications. Kidney Int 2011;79:708-14. https://doi.org/ 10.1038/ki.2010.432   DOI
53 Fritts CA, Waldroup PW. Effect of source and level of vitamin D on live performance and bone development in growing broilers. J Appl Poult Res 2003;12:45-52. https://doi.org/10.1093/japr/12.1.45   DOI
54 Pressman P, Clemens RA, Hayes AW. Bioavailability of micronutrients obtained from supplements and food: A survey and case study of the polyphenols. Toxicol Res Appl 2017;1: 1-7. https://doi.org/10.1177/2397847317696366
55 Garcia AFQM, Murakami AE, Duarte CRA, Rojas ICO, Picoli KP, Puzotti MM. Use of vitamin D3 and its metabolites in broiler chicken feed on performance, bone parameters and meat quality. Asian-Australas J Anim Sci 2013;26:408-15. https://doi.org/10.5713/ajas.2012.12455   DOI
56 Amundson LA. Insights into nutrient inputs that affect the initiation of bone lesions in pigs. J Anim Sci 2016;94(Suppl_2): 123.   DOI
57 Orban JI, Roland DA, Cummins K, Lovell RT. Influence of large doses of ascorbic acid on performance, plasma calcium, bone characteristics, and eggshell quality in broilers and Leghorn hens. Poult Sci 1993;72:691-700. https://doi.org/10.3382/ps.0720691   DOI
58 de Mendonca Jr CX, Guerra EM, Oliveria CA. Choline supplementation for Hisex Brown and Hisex White laying hens. 2. Liver lipid deposition and plasma lipids levels. Rev Fac Med Vet Zootec Univ S Paulo (Brazil) 1989;26:93-103.   DOI
59 National Research Council. Nutrient requirements of swine. 11th ed. Washington, DC, USA: National Academy Press; 2012.
60 Xu H, Dai S, Zhang K, et al. Dietary phosphorus deficiency impaired growth, intestinal digestion and absorption function of meat ducks. Asian-Australas J Anim Sci 2019;32:1897-906. https://doi.org/10.5713/ajas.18.0683   DOI
61 Fairweather-Tait, Southoun S. Bioavailability of nutrients. In: Caballero B, Trugo LC, Finglas PM, editors. Encyclopedia of food sciences and nutrition 2nd ed. London, UK: Academic Press; 2003. p. 478-84.
62 Ammerman CB, Baker DH, Lewis AJ. Bioavailability of nutrients for animals: amino acids, minerals, and vitamins. San Diego, CA, USA: Academic Press; 1995.
63 Sharma S, Jaiswal S, Duffy B, Jaiswal AK. Nanostructured materials for food applications: spectroscopy, microscopy and physical properties. Bioengineering 2019;6:26. https://doi.org/10.3390/bioengineering6010026   DOI
64 Gonnet M, Lethuaut L, Boury F. New trends in encapsulation of liposoluble vitamins. J Control Release 2010;146:276-90. https://doi.org/10.1016/j.jconrel.2010.01.037   DOI
65 Reza Mozafari M, Johnson C, Hatziantoniou S, Demetzos C. Nanoliposomes and their applications in food nanotechnology. J Liposome Res 2008;18:309-27. https://doi.org/10.1080/08982100802465941   DOI
66 Vahjen W, Zentek J, Durosoy S. Inhibitory action of two zinc oxide sources on the ex vivo growth of porcine small intestine bacteria. J Anim Sci 2012;90:334-6. https://doi.org/10.2527/ jas.52921   DOI
67 Cho JH, Upadhaya SD, Kim IH. Effects of dietary supplementation of modified zinc oxide on growth performance, nutrient digestibility, blood profiles, fecal microbial shedding and fecal score in weanling pigs. Anim Sci J 2015;86:617-23. https://doi.org/10.1111/asj.12329   DOI
68 Ghosh I, Bose S, Vippagunta R, Harmon F. Nanosuspension for improving the bioavailability of a poorly soluble drug and screening of stabilizing agents to inhibit crystal growth. Int J Pharm 2011;409:260-8. https://doi.org/10.1016/j.ijpharm.2011.02.051   DOI
69 Saltman PD, Strause LG. The role of trace minerals in osteoporosis. J Am Coll Nutr 1993;12:384-9. https://doi.org/10.1080/07315724.1993.10718327   DOI
70 Pepa GD, Brandi ML. Microelements for bone boost: the last but not the least. Clin Cases Miner Bone Metab 2016;13:181-5. https://doi.org/10.11138/ccmbm/2016.13.3.181
71 Reid DM, New SA. Nutritional influences on bone mass. Proc Nutr Soc 1997;56:977-87. https://doi.org/10.1079/PNS19970103   DOI
72 Palacios C. The role of nutrients in bone health, from A to Z. Crit Rev Food Sci Nutr 2006;46:621-8. https://doi.org/10.1080/10408390500466174   DOI
73 Peacock M. Calcium metabolism in health and disease. Clin J Am Soc Nephrol 2010;5(Suppl 1):S23-30. https://doi.org/ 10.2215/CJN.05910809   DOI
74 Shapiro R, Heaney RP. Co-dependence of calcium and phosphorus for growth and bone development under conditions of varying deficiency. Bone 2003;32:532-40. https://doi.org/10.1016/S8756-3282(03)00060-7   DOI
75 Lagos LV, Lee SA, Fondevila G, et al. Influence of the concentration of dietary digestible calcium on growth performance, bone mineralization, plasma calcium, and abundance of genes involved in intestinal absorption of calcium in pigs from 11 to 22 kg fed diets with different concentrations of digestible phosphorus. J Anim Sci Biotechnol 2019;10:47. https://doi.org/10.1186/s40104-019-0349-2   DOI
76 Tanck E, Homminga J, Van Lenthe GH, Huiskes R. Increase in bone volume fraction precedes architectural adaptation in growing bone. Bone 2001;28:650-4. https://doi.org/10.1016/S8756-3282(01)00464-1   DOI
77 Sommerville BA, Maunder E, Ross R, Care AD, Brown RC. Effect of dietary calcium and phosphorus depletion on vitamin D metabolism and calcium binding protein in the growing pig. Horm Metab Res 1985;17:78-81. https://doi.org/10.1055/s-2007-1013456   DOI
78 Heyer CME, Weiss E, Schmucker S, et al. The impact of phosphorus on the immune system and the intestinal microbiota with special focus on the pig. Nutr Res Rev 2015;28:67-82. https://doi.org/10.1017/S0954422415000049   DOI
79 Eklou-Kalonji E, Zerath E, Colin C, et al. Calcium-regulating hormones, bone mineral content, breaking load and trabecular remodeling are altered in growing pigs fed calcium-deficient diets. J Nutr 1999;129:188-93. https://doi.org/10.1093/jn/129.1.188   DOI
80 Sorensen KU, Tauson AH, Poulsen HD. Long term differentiated phosphorus supply from below to above requirement affects nutrient balance and retention, body weight gain and bone growth in growing-finishing pigs. Livest Sci 2018;211: 14-20. https://doi.org/10.1016/j.livsci.2018.03.002   DOI
81 Takayanagi H. Osteoimmunology: Shared mechanisms and crosstalk between the immune and bone systems. Nat Rev Immunol 2007;7:292-304. https://doi.org/10.1038/nri2062   DOI
82 Dacey MJ. Hypomagnesemic disorders. Crit Care Clin 2001; 17:155-73. https://doi.org/10.1016/S0749-0704(05)70157-3   DOI
83 Uwitonze AM, Razzaque MS. Role of magnesium in vitamin D activation and function. J Am Osteopath Assoc 2018;118: 181-9. https://doi.org/10.7556/jaoa.2018.037   DOI
84 Brown SE. Key minerals for bone health - magnesium. Bone nutrition [Internet]. c2014 [cited 2019, Oct, 15]. Available from https://www.betterbones.com/bone-nutrition/magnesium/
85 Rude RK, Singer FR, Gruber HE. Skeletal and hormonal effects of magnesium deficiency. J Am Coll Nutr 2009;28:131-41. https://doi.org/10.1080/07315724.2009.10719764   DOI
86 Bost M, Houdart S, Oberli M, Kalonji E, Huneau JF, Margaritis I. Dietary copper and human health: current evidence and unresolved issues. J Trace Elem Med Biol 2016;35:107-15. https://doi.org/10.1016/j.jtemb.2016.02.006   DOI
87 Zheng J, Mao X, Ling J, He Q, Quan J. Low serum levels of zinc, copper, and iron as risk factors for osteoporosis: a meta-analysis. Biol Trace Elem Res 2014;160:15-23. https://doi.org/10.1007/s12011-014-0031-7   DOI
88 Aaseth J, Boivin G, Andersen O. Osteoporosis and trace elements - an overview. J Trace Elem Med Biol 2012;26:149-52. https://doi.org/10.1016/j.jtemb.2012.03.017   DOI
89 Rondanelli M, Opizzi A, Perna S, Faliva MA. Update on nutrients involved in maintaining healthy bone. Endocrinol Nutr 2013;60:197-210. https://doi.org/10.1016/j.endonu.2012.09.006   DOI
90 Patrick L. Comparative absorption of calcium sources and calcium citrate malate for the prevention of osteoporosis. Altern Med Rev 1999;4:74-85.
91 Rico H, Roca-Botran C, Hernandez ER, et al. The effect of supplemental copper on osteopenia induced by ovariectomy in rats. Menopause 2000;7:413-6. https://doi.org/10.1097/00042192-200011000-00007   DOI
92 Pietak AM, Reid JW, Stott MJ, Sayer M. Silicon substitution in the calcium phosphate bioceramics. Biomaterials 2007;28:4023-32. https://doi.org/10.1016/j.biomaterials.2007.05.003   DOI
93 Volpe S, Taper LJ, Meacham S. The relationship between boron and magnesium status and bone mineral density in the human: a review. Magnes Res 1993;6:291-6.
94 Maehira F, Miyagi I, Eguchi Y. Effects of calcium sources and soluble silicate on bone metabolism and the related gene expression in mice. Nutrition 2009;25:581-9. https://doi.org/10.1016/j.nut.2008.10.023   DOI
95 Short FE, Burton E, Belton D, Mann G, Perry C. Efficacy of a novel form of dietary silicon supplement in reducing lameness in poultry. Br Poult Abstr 2011;7:1-2.   DOI
96 Nakhon S, Numthuam S, Charoensook R, Tartrakoon W, Incharoen P, Incharoen T. Growth performance, meat quality, and bone-breaking strength in broilers fed dietary rice hull silicon. Anim Nutr 2019;5:152-5. https://doi.org/10.1016/j.aninu.2018.11.003   DOI
97 Penland JG. Dietary boron, brain function, and cognitive performance. Environ Health Perspect 1994;102(Suppl 7):S65-72. https://doi.org/10.1289/ehp.94102s765
98 Institute of Medicine. Dietary reference intakes for vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium, and zinc. Washington, DC, USA: The National Academies Press; 2001. https://doi.org/10.17226/10026
99 Guo HH, Hong ZA, Yi RZ. Core-shell collagen peptide chelated calcium/calcium alginate nanoparticles from fish scales for calcium supplementation. J Food Sci 2015;80:N1595-601. https://doi.org/10.1111/1750-3841.12912   DOI
100 Cao J, Henry PR, Davis SR, et al. Relative bioavailability of organic zinc sources based on tissue zinc and metallothionein in chicks fed conventional dietary zinc concentrations. Anim Feed Sci Technol 2002;101:161-70. https://doi.org/10.1016/S0377-8401(02)00051-2   DOI
101 Chen J, Qiu X, Hao G, Zhang M, Weng W. Preparation and bioavailability of calcium-chelating peptide complex from tilapia skin hydrolysates. J Sci Food Agric 2017;97:4898-903. https://doi.org/10.1002/jsfa.8363   DOI
102 Yi G, Atwell C, Hume J, Dibner J, Knight C, Richards J. Determining the methionine activity of Mintrex organic trace minerals in broiler chicks by using radiolabel tracing or growth assay. Poult Sci 2007;86:877-87. https://doi.org/10.1093/ps/86.5.877   DOI
103 Sun Q, Guo Y, Li J, Zhang T, Wen J. Effects of methionine hydroxy analog chelated Cu/Mn/Zn on laying performance, egg quality, enzyme activity and mineral retention of laying hens. J Poult Sci 2012;49:20. https://doi.org/10.2141/jpsa. 011055   DOI
104 Bollengier-Lee S, Mitchell MA, Utomo DB, Williams PEV, Whitehead CC. Influence of high dietary vitamin E supplementation on egg production and plasma characteristics in hens subjected to heat stress. Br Poult Sci 1998;39:106-12. https://doi.org/10.1080/00071669889466   DOI
105 Manangi MK, Hampton T, Fisher P, Richards JD, Vazquez-Anon M, Christensen KD. Impact of feeding lower levels of chelated trace minerals vs. industry levels of inorganic trace minerals on broiler performance, yield, footpad health, and litter mineral concentration. J Appl Poult Res 2012;21:881-90. https://doi.org/10.3382/japr.2012-00531   DOI
106 DSM Nutritional Products Limited. Optimum vitamin nutrition: in the production of quality animal foods. Benchmark House, UK: 5m Publishing; 2012.
107 Lin H, Wang LF, Song JL, Xie YM, Yang QM. Effect of dietary supplemental levels of vitamin a on the egg production and immune responses of heat-stressed laying hens. Poult Sci 2002;81:458-65. https://doi.org/10.1093/ps/81.4.458   DOI
108 Mattila P, Valaja J, Rossow L, Venalainen E, Tupasela T. Effect of vitamin D2- and D3- enriched diets on egg vitamin D content, production, and bird condition during an entire production period. Poult Sci 2004;83:433-40. https://doi.org/10.1093/ps/83.3.433   DOI
109 Terry M, Lanenga M, McNaughton JL, Stark LE. Safety of 25-hydrioxyvitamin $D_{3}$ as a source of vitamin $D_{3}$ in layer poultry feed. Vet Hum Toxicol 1999;41:312-6.
110 Fleming RH, McCormack HA, Whitehead CC. Bone structure and strength at different ages in laying hens and effects of dietary particulate limestone, vitamin K and ascorbic acid. Br Poult Sci 1998;39:434-40. https://doi.org/10.1080/00071669889024   DOI
111 Squires MW, Naber EC. Vitamin profiles of eggs as indicators of nutritional status in the laying hen: riboflavin study. Poult Sci 1993;72:483-94. https://doi.org/10.3382/ps.0720483   DOI