2,504
Views
8
CrossRef citations to date
0
Altmetric
Nutrition & Metabolism

Dietary betaine reduces plasma homocysteine concentrations and improves bone strength in laying hens

, , , , & ORCID Icon
Pages 573-578 | Received 27 Jul 2020, Accepted 04 Jan 2021, Published online: 03 Mar 2021

References

  • Bar, A. 2009. “Calcium Transport in Strongly Calcifying Laying Birds: Mechanisms and Regulation.” Comparative Biochemistry and Physiology A: Molecular & Integrative Physiology 152: 447–469. doi:10.1016/j.cbpa.2008.11.020.
  • Beck, M. M., and K. K. Hansen. 2004. “Role of Estrogen in Avian Osteoporosis.” Poultry Science 83: 200–206. doi:10.1093/ps/83.2.200.
  • Berendsen, A. D., and B. R. Olsen. 2015. “Bone Development.” Bone 80: 14–18. doi:10.1016/j.bone.2015.04.035.
  • Bishop, S. C., R. H. Fleming, H. A. Mccormack, D. K. Flock, and C. C. Whitehead. 2000. “Inheritance of Bone Characteristics Affecting Osteoporosis in Laying Hens.” British Poultry Science 41: 33–40. doi:10.1080/00071660086376.
  • Blouin, S., H. W. Thaler, C. Korninger, R. Schmid, J. G. Hofstaetter, R. Zoehrer, R. Phipps, K. Klaushofer, P. Roschger, and E. P. Paschalis. 2009. “Bone Matrix Quality and Plasma Homocysteine Levels.” Bone 44: 959–964. doi:10.1016/j.bone.2008.12.023.
  • Bourckhardt, G. F., M. S. Cecchini, M. L. D. Hahmeyer, A. P. Remor, A. Latini, D. Ammar, Y. M. R. Muller, and E. M. Nazari. 2019. “Impact of Homocysteine on Vasculogenic Factors and Bone Formation in Chicken Embryos.” Cell Biology and Toxicology 35: 49–58. doi:10.1007/s10565-018-9436-y.
  • Chesson, A. 1993. “Feed Enzymes.” Animal Feed Science and Technology 45: 65–79. doi:10.1016/0377-8401(93)90072-r.
  • Clark, W. D., W. R. Cox, and F. G. Silversides. 2008. “Bone Fracture Incidence in End-of-lay High-producing, Noncommercial Laying Hens Identified Using Radiographs.” Poultry Science 87: 1964–1970. doi:10.3382/ps.2008-00115.
  • Clark, W. D., E. L. Smith, K. A. Linn, J. R. Paul-Murphy, and M. E. Cook. 2005. “Use of Peripheral Quantitative Computed Tomography to Monitor Bone Healing after Radial Osteotomy in Three-week-old Chickens (Gallus Domesticus).” Journal of Avian Medicine and Surgery 19: 198–207. doi:10.1647/2003-037.1.
  • Cowieson, A. J., and O. Adeola. 2011. “Board-invited Review: Opportunities and Challenges in Using Exogenous Enzymes to Improve Nonruminant Animal Production.” Journal of Animal Science 89: 3189–3218. doi:10.2527/jas.2010-3715.
  • Cowieson, A. J., P. Wilcock, and M. R. Bedford. 2011. “Super-dosing Effects of Phytase in Poultry and Other Monogastrics.” Worlds Poultry Science Journal 67: 225–235. doi:10.1017/s0043933911000250.
  • Craig, S. A. S. 2004. “Betaine in Human Nutrition.” American Journal of Clinical Nutrition 80: 539–549. doi:10.1093/ajcn/80.3.539.
  • Dacke, C. G., S. Arkle, D. J. Cook, I. M. Wormstone, S. Jones, M. Zaidi, and Z. A. Bascal. 1993. “Medullary Bone and Avian Calcium Regulation.” Journal of Experimental Biology 184: 63–88.
  • De Koning, D. J., N. Dominguez-Gasca, R. H. Fleming, A. Gill, D. Kurian, A. Law, H. A. Mccormack, et al. 2020. “An eQTL in the Cystathionine Beta Synthase Gene Is Linked to Osteoporosis in Laying Hens.” Genetics Selection Evolution 52. doi:10.1186/s12711-020-00532-y.
  • Dimeglio, L. A., and E. A. Imel. 2019. “Calcium and Phosphate: Hormonal Regulation and Metabolism.” In Basic and Applied Bone Biology, edited by M. R. ALLEN and D. B. BURR, 257–282. London: Waltham, MA, Academic Press.
  • Dunn, I. C., R. H. Fleming, H. A. Mccormack, D. Morrice, D. W. Burt, R. Preisinger, and C. C. Whitehead. 2007. “A QTL for Osteoporosis Detected in an F-2 Population Derived from White Leghorn Chicken Lines Divergently Selected for Bone Index.” Animal Genetics 38: 45–49. doi:10.1111/j.1365-2052.2006.01547.x.
  • Eklund, M., E. Bauer, J. Wamatu, and R. Mosenthin. 2005. “Potential Nutritional and Physiological Functions of Betaine in Livestock.” Nutrition Research Reviews 18: 31–48. doi:10.1079/Nrr200493.
  • Finkelstein, J. D. 1998. “The Metabolism of Homocysteine: Pathways and Regulation.” European Journal of Pediatrics 157: S40–S44. doi:10.1007/pl00014300.
  • Fleming, R. H. 2008. “Nutritional Factors Affecting Poultry Bone Health.” Proceedings of the Nutrition Society 67: 177–183. doi: 10.1017/s0029665108007015.
  • Fleming, R. H., H. A. Mccormack, L. Mcteir, and C. C. Whitehead. 1998b. “Medullary Bone and Humeral Breaking Strength in Laying Hens.” Research in Veterinary Science 64: 63–67. doi:10.1016/S0034-5288(98)90117-5.
  • Fleming, R. H., H. A. Mccormack, L. Mcteir, and C. C. Whitehead. 2006. “Relationships between Genetic, Environmental and Nutritional Factors Influencing Osteoporosis in Laying Hens.” British Poultry Science 47: 742–755. doi:10.1080/00071660601077949.
  • Fleming, R. H., H. A. Mccormack, and C. C. Whitehead. 1998a. “Bone Structure and Strength at Different Ages in Laying Hens and Effects of Dietary Particulate Limestone, Vitamin K and Ascorbic Acid.” British Poultry Science 39: 434–440. doi:10.1080/00071669889024.
  • Freire, R., L. J. Wilkins, F. Short, and C. J. Nicol. 2003. “Behaviour and Welfare of Individual Laying Hens in a Non-cage System.” British Poultry Science 44: 22–29. doi:10.1080/0007166031000085391.
  • Haldar, S., A. Singh, T. Ghosh, and D. Creswell. 2015. “Effects of Supplementation of Betaine Hydrochloride on Physiological Performances of Broilers Exposed to Thermal Stress.” Open Access Animal Physiology 111. doi:10.2147/oaap.s83190.
  • Herrmann, M., A. Tami, B. Wildemann, M. Wolny, A. Wagner, H. Schorr, O. Taban-Shomal, et al. 2009. “Hyperhomocysteinemia Induces a Tissue Specific Accumulation of Homocysteine in Bone by Collagen Binding and Adversely Affects Bone.” Bone 44: 467–475. doi:10.1016/j.bone.2008.10.051.
  • Herrmann, M., T. Widmann, G. Colaianni, S. Colucci, A. Zallone, and W. Herrmann. 2005. “Increased Osteoclast Activity in the Presence of Increased Homocysteine Concentrations.” Clinical Chemistry 51: 2348–2353. doi:10.1373/clinchem.2005.053363.
  • Holstein, J. H., M. Herrmann, C. Splett, W. Herrmann, P. Garcia, T. Histing, M. Klein, et al. 2011. “High Bone Concentrations of Homocysteine are Associated with Altered Bone Morphology in Humans.” British Journal of Nutrition 106: 378–382. doi:10.1017/S0007114511000304.
  • Jhee, K. H., and W. D. Kruger. 2005. “The Role of Cystathionine Beta-synthase in Homocysteine Metabolism.” Antioxidants & Redox Signaling 7: 813–822. doi:10.1089/ars.2005.7.813.
  • Kang, S. S., P. W. K. Wong, and M. R. Malinow. 1992. “Hyperhomocyst(E)Inemia AS A Risk Factor for Occlusive Vascular-Disease.” Annual Review of Nutrition 12: 279–298. doi:10.1146/annurev.nutr.12.1.279.
  • Kerschnitzki, M., T. Zander, P. Zaslansky, P. Fratzl, R. Shahar, and W. Wagermaier. 2014. “Rapid Alterations of Avian Medullary Bone Material during the Daily Egg-laying Cycle.” Bone 69: 109–117. doi:10.1016/j.bone.2014.08.019.
  • Kim, J. H., F. M. Pitargue, H. Jung, G. P. Han, H. S. Choi, and D. Y. Kil. 2017. “Effect of Superdosing Phytase on Productive Performance and Egg Quality in Laying Hens.” Asian-Australasian Journal of Animal Sciences 30: 994–998. doi:10.5713/ajas.17.0149.
  • Koh, J. M., Y. S. Lee, Y. S. Kim, D. J. Kim, H. H. Kim, J. Y. Park, K. U. Lee, and G. S. Kim. 2006. “Homocysteine Enhances Bone Resorption by Stimulation of Osteoclast Formation and Activity through Increased Intracellular ROS Generation.” Journal of Bone and Mineral Research 21: 1003–1011. doi:10.1359/jbmr.060406.
  • Li, J., M. A. Kacena, and D. L. Stocum. 2019. “Fracture Healing.” In Basic and Applied Bone Biology, edited by M. R. Allen and D. B. Burr, 235–253. London: Waltham, MA, Academic Press.
  • Lohmann Tierzucht GmbH. 2018. Lohmann LSL-Lite Management Guide. Vol. 2019. Germany: Lohmann Tierzucht GmbH. https://www.ltz.de.
  • Masse, P. G., A. L. Boskey, I. Ziv, P. Hauschka, S. M. Donovan, D. S. Howell, and D. E. C. Cole. 2003. “Chemical and Biomechanical Characterization of Hyperhomocysteinemic Bone Disease in an Animal Model.” BMC Musculoskeletal Disorders 4. doi:10.1186/1471-2474-4-2.
  • Masse, P. G., C. M. Rimnac, M. Yamauchi, S. P. Coburn, R. B. Rucker, D. S. Howell, and A. L. Boskey. 1996. “Pyridoxine Deficiency Affects Biomechanical Properties of Chick Tibial Bone.” Bone 18: 567–574. doi:10.1016/8756-3282(96)00072-5.
  • Nicol, C. J., S. N. Brown, E. Glen, S. J. Pope, F. J. Short, P. D. Warriss, P. H. Zimmerman, and L. J. Wilkins. 2006. “Effects of Stocking Density, Flock Size and Management on the Welfare of Laying Hens in Single-tier Aviaries.” British Poultry Science 47: 135–146. doi:10.1080/00071660600610609.
  • Petrik, M. T., M. T. Guerin, and T. M. Widowski. 2015. “On-farm Comparison of Keel Fracture Prevalence and Other Welfare Indicators in Conventional Cage and Floor-housed Laying Hens in Ontario, Canada.” Poultry Science 94: 579–585. doi:10.3382/ps/pev039.
  • Petronini, P. G., E. M. De Angelis, P. Borghetti, A. F. Borgetti, and K. P. Wheeler. 1992. “Modulation by Betaine of Cellular Responses to Osmotic Stress.” Journal of Biological Chemistry 282: 5.
  • Raymond, B., A. M. Johansson, H. A. Mccormack, R. H. Fleming, M. Schmutz, I. C. Dunn, and D. J. De Koning. 2018. “Genome-wide Association Study for Bone Strength in Laying Hens.” Journal of Animal Science 96: 2525–2535. doi:10.1093/jas/sky157.
  • Rojas, I. Y. M., C. L. Coello, E. A. Gonzalez, J. A. Menocal, and G. A. Gomes. 2018. “Effect of Phytase Dose on Productive Performance and Bone Status of Layers Fed with Graded Levels of Digestible Lysine.” Veterinaria Mexico 5. doi:10.22201/fmvz.24486760e.2018.3.564.
  • Selle, P. H., and V. Ravindran. 2007. “Microbial Phytase in Poultry Nutrition.” Animal Feed Science and Technology 135: 1–41. doi:10.1016/j.anifeedsci.2006.06.010.
  • Simon, J. 1999. “Choline, Betaine and Methionine Interactions in Chickens, Pigs and Fish (Including Crustaceans).” Worlds Poultry Science Journal 55: 353–374. doi:10.1079/Wps19990025.
  • Taylor, A. E., M. R. Bedford, S. C. Pace, and H. M. Miller. 2018. “The Effects of Phytase and Xylanase Supplementation on Performance and Egg Quality in Laying Hens.” British Poultry Science 59: 554–561. doi:10.1080/00071668.2018.1483575.
  • Thaler, R., M. Agsten, S. Spitzer, E. P. Paschalis, H. Karlic, K. Klaushofer, and F. Varga. 2011. “Homocysteine Suppresses the Expression of the Collagen Cross-linker Lysyl Oxidase Involving IL-6, Fli1, and Epigenetic DNA Methylation.” Journal of Biological Chemistry 286: 5578–5588. doi:10.1074/jbc.M110.166181.
  • Toscano, M. J., I. C. Dunn, J. P. Christensen, S. Petow, K. Kittelsen, and R. Ulrich. 2020. “Explanations for Keel Bone Fractures in Laying Hens: Are There Explanations in Addition to Elevated Egg Production?” Poultry Science 99: 4183–4194. doi:10.1016/j.psj.2020.05.035.
  • Van Meurs, J. B. J., R. A. M. Dhonukshe-Rutten, S. M. F. Pluijm, M. Van Der Klift, R. De Jonge, J. Lindemans, L. De Groot, et al. 2004. “Homocysteine Levels and the Risk of Osteoporotic Fracture.” New England Journal of Medicine 350: 2033–2041. doi:10.1056/NEJMoa032546.
  • Whitehead, C. C. 2004. “Overview of Bone Biology in the Egg-laying Hen.” Poultry Science 83: 193–199. doi:10.1093/ps/83.2.193.
  • Whitehead, C. C., and R. H. Fleming. 2000. “Osteoporosis in Cage Layers.” Poultry Science 79: 1033–1041. doi:10.1093/ps/79.7.1033.
  • Wilkins, L. J., S. N. Brown, P. H. Zimmerman, C. Leeb, and C. J. Nicol. 2004. “Investigation of Palpation as a Method for Determining the Prevalence of Keel and Furculum Damage in Laying Hens.” Veterinary Record 155: 547–549. doi:10.1136/vr.155.18.547.
  • Wilkins, L. J., J. L. Mckinstry, N. C. Avery, T. G. Knowles, S. N. Brown, J. Tarlton, and C. J. Nicol. 2011. “Influence of Housing System and Design on Bone Strength and Keel Bone Fractures in Laying Hens.” Veterinary Record 169: 414. doi:10.1136/vr.d4831.
  • Zhou, J., J. Moller, C. C. Danielsen, J. Bentzon, H. B. Ravn, R. C. Austin, and E. Falk. 2001. “Dietary Supplementation with Methionine and Homocysteine Promotes Early Atherosclerosis but Not Plaque Rupture in apoE-deficient Mice.” Arteriosclerosis, Thrombosis, and Vascular Biology 21: 1470–1476. doi:10.1161/hq0901.096582.