Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
권호 표지
DOI QR코드

DOI QR Code

Metabolic, Osmoregulatory and Nutritional Functions of Betaine in Monogastric Animals

  • Ratriyanto, A. (Institute of Animal Nutrition, University of Hohenheim) ;
  • Mosenthin, R. (Institute of Animal Nutrition, University of Hohenheim) ;
  • Bauer, E. (Institute of Animal Nutrition, University of Hohenheim) ;
  • Eklund, M. (Institute of Animal Nutrition, University of Hohenheim)
  • Received : 2008.11.28
  • Accepted : 2009.03.05
  • Published : 2009.10.01
Download PDF
⟨ Previous Next ⟩

Abstract

This review focuses on the metabolic and osmoregulatory functions of betaine and its impact on nutrient digestibility and performance in pigs and poultry. Betaine is the trimethyl derivative of the amino acid glycine, and is present in plant and animal tissue. It has been shown to play an important role in osmoregulation of plants, bacteria and marine organisms. Due to its chemical structure, betaine exerts a number of functions both at the gastrointestinal and metabolic level. As a methyl group donor, betaine is involved in transmethylation reactions and donates its labile methyl group for the synthesis of several metabolically active substances such as creatine and carnitine. Therefore, supplementation of betaine may reduce the requirement for other methyl group donors such as methionine and choline. Beneficial effects on intestinal cells and intestinal microbes have been reported following betaine supplementation to diets for pigs and poultry, which have been attributed to the osmotic properties of betaine. Furthermore, betaine potentially enhances the digestibility of specific nutrients, in particular fiber and minerals. Moreover, at the metabolic level, betaine is involved in protein and energy metabolism. Growth trials revealed positive effects of supplemental betaine on growth performance in pigs and poultry, and there is evidence that betaine acts as a carcass modifier by reducing the carcass fat content. In conclusion, due to its various metabolic and osmoregulatory functions, betaine plays an important role in the nutrition of monogastric animals.

Keywords

References

  1. Alaviuhkola, T. and K. Suomi. 1990, Effect of betaine supplementation of low methionine diet for growing pigs, Ann.Agric. Fenn 29:127-129
  2. Attia, Y. A., R. A. Hassan, M. H. Shehatta and S. B. Abd-El-Hady. 2005, Growth, carcass quality and serum constituents of slow growing chicks as affected by betaine addition to diets containing 2. Different levels of methionine, Int. J. Poult. Sci4:856-865 https://doi.org/10.3923/ijps.2005.856.865
  3. Augustine, P. C. and H. D. Danforth. 1999, Influence of betaine and salinomycin on intestinal absorption of methionine and glucose and on the ultrastructure of intestinal cells and parasite developmental stages in chicks infected with Eimeria acervulina, Avian Dis 43:89-97 https://doi.org/10.2307/1592766
  4. Augustine, P. C., J. L. McNaughton, E. Virtanen and L. Rosi. 1997, Effect of betaine on the growth performance of chicks inoculated with mixed cultures of avian Eimeria species and on invasion and development of Eimeria tenella and Eimeria acervulina in vitro and in vivo, Poult. Sci 76:802-809
  5. Aulrich, K. and G. Flachowsky. 1997. Wirksamkeit NSPspaltender Enzyme - in vitro-Studien an Modellfuttermitteln. In: Vitamine und Zusatzstoffe in der Ern$\ddot{a}$hrung von Mensch und Tier (Ed. R. Schubert, G. Flachowsky, R. Bitsch and G Jahreis). 6. Symposium, Jena/Th$\ddot{u}$ringen, Weimar Kessler GmbH, Germany. pp. 322-328
  6. Biggers, J. D., J. A. Lawitts and C. P. Lechene. 1993, The protective action of betaine on the deleterious effects of NaCl on preimplantation mouse embryos in vitro, Mol. Reprod. Develop 34:380-390 https://doi.org/10.1002/mrd.1080340406
  7. Boch, J., B. Kempf and E. Bremer. 1994, Osmoregulation in Bacillus subtilis: synthesis of the osmoprotectant glycine betaine from exogenously provided choline, J. Bacteriol 176:5364-5371
  8. Butzner, J. D., J. B. Meddings and V. Dalal. 1994, Inhibition of short-chain fatty acid absorption and Na+ absorption during acute colitis in the rabbit, Gastroenterology 106:1190-1198
  9. Cadogan, D. J., R. G. Campbell, D. Harrison and A. C. Edwards. 1993, The effects of betaine on the growth performance and carcass characteristics of female pigs. In: Manipulating Pig Production IV (Ed. E. S. Batterham). Australasian Pig Science Association, Attwood, Victoria, Australia. pp. 219-225
  10. Campbell, R. G., D. J. Cadogan, W. C. Morley, R. Uusitalo and E. Virtanen. 1995, Interrelationships between dietary methionine and betaine on the growth performance of pigs from 65 to 100 kg, J. Anim. Sci 73(Suppl. 1):82(Abstr.)
  11. Campbell, R. G., D.T. Harrison and P. Rich. 1997a, The effects of including betaine in the diet offered during lactation on the subsequent reproductive performance of sows. In: Manipulating pig production VI (Ed. P. D. Cranwell). Australasian Pig Science Association, Werribee, Victoria, Australia. p. 242
  12. Campbell, R. G., W. C. Morley and B. Zabaras-Krick. 1997b, The effects of betaine on protein and energy metabolism of growing pigs. In: Manipulating pig production VI (Ed. P. D. Cranwell). Australasian Pig Science Association, Werribee, Victoria, Australia. p. 243
  13. Cera, K. R. and A. P. Schinckel. 1995, Carcass and performance responses to feeding betaine in pigs, J. Anim. Sci 73(Suppl.1):82(Abstr.)
  14. Chambers, S. T. and C. M. Kunin. 1985, The osmoprotective properties of urine for bacteria: The protective effect of betaine and human urine against low pH and high concentrations of electrolytes, sugars, and urea, J. Infec. Dis 152:1308-1316 https://doi.org/10.1093/infdis/152.6.1308
  15. Chendrimada, T. P., M. G. Neto, G. M. Pesti, A. J. Davis and R. I. Bakalli. 2002, Determination of the betaine content of feed ingredients using high-performance liquid chromatography, J.Sci. Food Agric 82:1556-1563 https://doi.org/10.1002/jsfa.1214
  16. Clarke, W. C., E. Virtanen, J. Blackburn and D. A. Higgs. 1994, Effects of a dietary betaine/amino acid additive on growth and seawater adaptation in yearling chinook salmon, Aquaculture121:137-145 https://doi.org/10.1016/0044-8486(94)90015-9
  17. Clow, K. A., J. T. Treberg, M. E. Brosnan and J. T. Brosnan. 2008, Elevated tissue betaine contents in developing rats are due to dietary betaine, not to synthesis, J. Nutr 138:1641-1646
  18. Cromwell, G. L., M. D. Lindemann, J. R. Randolph, H. J. Monegue, K. M. Laurent and G. R. Parker. 1999, Efficacy of betaine as a carcass modifier in finishing pigs fed normal and reduced energy diets, J. Anim. Sci 77(Suppl. 1):179(Abstr.).
  19. Csonka, L. N. 1989, Physiological and genetic responses of bacteria to osmotic stress, Microbiol. Rev 53:121-147
  20. Dawson, K. M. and J. M. Baltz. 1997, Organic osmolytes and embryos: substrates of the Gly and $\beta$ transport systems protect mouse zygotes against the effects of raised osmolarity, Biol.Reprod 56:1550-1558 https://doi.org/10.1095/biolreprod56.6.1550
  21. Dilger, R. N., T. A. Garrow and D. H. Baker. 2007, Betaine can partially spare choline in chicks but only when added to diets containing a minimal level of choline, J. Nutr 137:2224-2228
  22. Dunshea, F. R., D. J. Cadogan and G. G. Partridge. 2007, Dietary betaine and ractopamine have additive effects on lean tissue deposition, particularly in restrictively-fed gilts. In: Manipulating pig production XI. (Eds. J. E. Paterson and J. A. Barker). Australasian Pig Science Association, Scott Print,Perth, Western Australia. p. 120
  23. Eklund, M., E. Bauer, J. Wamatu and R. Mosenthin. 2005, Potential nutritional and physiological functions of betaine in livestock, Nutr. Res. Rev 18:31-48 https://doi.org/10.1079/NRR200493
  24. Eklund, M., R. Mosenthin, M. Tafaj and J. Wamatu. 2006a, Effects of betaine and condensed molasses solubles on nitrogen balance and nutrient digestibility in piglets fed diets deficient in methionine and low in compatible osmolytes, Arch. Anim. Nutr 60:289-300 https://doi.org/10.1080/17450390600785525
  25. Eklund, M., R. Mosenthin and H. P. Piepho. 2006b, Effects of betaine and condensed molasses solubles on ileal and total tract nutrient digestibilities in piglets, Acta Agric. Scand. Section A 56:83-90 https://doi.org/10.1080/09064700600979743
  26. El-Husseiny, O. M., M. A. Abo-El-Ella, M. O. Abd-Elsamee and M. M. Ab-Elfattah. 2007, Response of broilers performance to dietary betaine and folic acid at different methionine levels, Int. J. Poult. Sci 6:515-523 https://doi.org/10.3923/ijps.2007.515.523
  27. Emmert, J. L. and D. H. Baker. 1997, A chick bioassay approach for determining the bioavailability choline concentration in normal and overheated soybean meal, canola meal and peanut meal, J. Nutr 127:745-752 https://doi.org/10.1016/S0955-2863(97)00115-0
  28. Emmert, J. L., T. A. Garrow and D. H. Baker. 1996, Hepatic betaine-homocysteine methyltransferase activity in the chicken is influenced by dietary intake of sulfur amino acids, choline and betaine, J. Nutr 126:2050-2058
  29. Emmert, J. L., D. M. Webel, R. R. Biehl, M. A. Griffiths, L. S. Garrow, T. A. Garrow and D. H. Baker. 1998, Hepatic and renal betaine-homocysteine methyltransferase activity in pigs as affected by dietary intakes of sulfur amino acids, choline and betaine, J. Anim. Sci 76:606-610
  30. Esteve-Garcia, E. and S. Mack. 2000, The effect of DL-methionine and betaine on growth performance and carcass characteristics in broilers, Anim. Feed Sci Technol. 87:85-93 https://doi.org/10.1016/S0377-8401(00)00174-7
  31. Farooqi, H. A. G., M. S. Khan, M. A. Khan, M. Rabbani, K. Pervez and J. A. Khan. 2005, Evaluation of betaine and vitamin C in alleviation of heat stress in broilers, Int. J. Agric. Biol 5:744-746
  32. Feng, J., X. Liu, Y. Z. Wang and Z. R. Xu. 2006, Effects of betaine on performance, carcass characteristics and hepatic betainehomocysteine methyltransferase activity in finishing barrows, Asian-Aust. J. Anim. Sci 19:402-405
  33. Feng, J. and D. Y. Yu. 2001, Effect of betaine on growth performance and methyl transfer function in finisher pigs, Chin. J. Anim. Sci 37:8-10
  34. Fernandez-Figares, I., D. Wray-Cahen, N. C. Steele, R. G. Campbell, D. D. Hall, E. Virtanen and T. J. Caperna. 2002, Effect of dietary betaine on nutrient utilization and partitioning in the young growing feed-restricted pig, J. Anim. Sci 80:421-428
  35. Fernandez-Figares, I., J. A. Conde-Aguilera, R. Nieto, M. Lachica and J. F. Aguilera. 2008, Synergistic effects of betaine and conjugated linoleic acid on growth and carcass composition of growing Iberian pigs, J. Anim. Sci 86:102-111 https://doi.org/10.2527/jas.2006-0230
  36. Finkelstein, J. D. 1998, The metabolism of homocysteine: Pathways and regulation, Eur. J. Pediatr 157 (Suppl. 2):S40- S44 https://doi.org/10.1007/PL00014300
  37. Finkelstein, J. D. and S. H. Mudd. 1967, Trans-sulfuration in mammals: The methionine-sparing effect of cystine, J. Biol.Chem 242:873-880
  38. Finkelstein, J. D. and J. J. Martin. 1984, Methionine metabolism in mammals. Distribution of homocysteine between competing pathways, J. Biol. Chem 259:9508-9513
  39. Garcia, M. N., T. P. Chendrimada, G. M. Pesti and R. I. Bakalli. 1999, Relative bioavailability of two labile methyl sources methionine and betaine, Poult. Sci 78(Suppl. 1):87(Abstr.) https://doi.org/10.1002/jsfa.1214
  40. Glaasker, E., W. N. Konings and B. Poolman. 1996, Osmotic regulation of intracellular solute pools in Lactobacillus plantarum, J. Bacteriol 178:575-582
  41. Gu, X. and D. Li. 2003, Fat nutrition and metabolism in piglets: A review. Anim. Feed Sci. Technol 109:151-170 https://doi.org/10.1016/S0377-8401(03)00171-8
  42. Hall, D. D., D. E. Orr, Jr., M. E. Wilson, R. L. Moser and K. A. Whittington. 1997, Effect of betaine in finishing pig diets, J. Anim. Sci 75(Suppl. 1):75(Abstr.)
  43. Hammer, M. A. and J. M. Baltz. 2002, Betaine is a highly effective organic osmolyte but does not appear to be transported by established organic osmolyte transporters in mouse embryos, Mol. Reprod. Develop 62:195-202 https://doi.org/10.1002/mrd.10088
  44. Hanczakowska, E., J. Urbanczyk and M. Swiatkiewicz. 1999, The efficiency of betaine and organic compounds of chromium in fattening of pigs with ad libitum or restricted feeding, Rocz. Nauk. Zoot 26:263-274
  45. Hassan, R. A., Y. A. Attia and E. H. El-Ganzory. 2005, Growth, carcass quality and serum constituents of slow growing chicks as affected by betaine addition to diets containing 1. Different levels of choline, Int. J. Poult. Sci 4:840-850 https://doi.org/10.3923/ijps.2005.840.850
  46. H$\ddot{a}$ussinger, D. 1998, Osmoregulation of liver cell function: Signalling, osmolytes and cell heterogeneity, Contrib. Nephrol 123:185-204 https://doi.org/10.1159/000059913
  47. Hochachka, P. W. and G. N. Somero. 1984, Biochemical Adaptation, Princeton University Press, Princeton, NJ, USA
  48. Honarbakhsh, S., M. Zaghari and M. Shivazad. 2007a, Can exogenous betaine be an effective osmolyte in broiler chicks under water salinity stress? Asian-Aust. J. Anim. Sci 20:1729-1737
  49. Honarbakhsh, S., M. Zaghari and M. Shivayad. 2007b, Interactive effects of dietary betaine and saline water on carcass traits of broiler chicks, J. Biol. Sci 7:1208-1214 https://doi.org/10.3923/jbs.2007.1208.1214
  50. Hruby, M., A. Ombabi and A. Schlagheck. 2005, Natural betaine maintains layer performance in methionine/choline chloride reduced diets. Proceedings of the 15th European Symposium on Poultry Nutrition, World's Poultry Science Association, Hungarian Branch. Balatonf$\ddot{u}$red, Hungary. pp. 487-489
  51. Huang, Q. C., Z. R. Xu, X. Y. Han and W. F. Li. 2006, Changes in hormones, growth factor and lipid metabolism in finishing pigs fed betaine, Livest. Sci 105:78-85 https://doi.org/10.1016/j.livsci.2006.04.031
  52. Huang, Q. C., Z. R. Xu, X. Y. Han and W. F. Li. 2007, Effect of betaine on growth hormone pulsatile secretion and serum metabolites in finishing pigs, J. Anim. Physiol. Anim. Nutr 91:85-90 https://doi.org/10.1111/j.1439-0396.2006.00644.x
  53. Huang, Q. C., Z. R. Xu, X. Y. Han and W. F. Li. 2008, Effect of dietary betaine supplementation on lipogenic enzyme activities and fatty acid synthase mRNA expression in finishing pigs, Anim. Feed Sci. Technol 140:365-375 https://doi.org/10.1016/j.anifeedsci.2007.03.007
  54. Hur, S. J., H. S. Yang, G. B. Park and S. T. Joo. 2007, Effects of dietary glycine betaine on pork quality in different muscle types, Asian-Aust. J. Anim. Sci 20:1754-1760
  55. Hutkins, R. W., W. L. Ellefson and E. R. Kashket. 1987, Betaine transport imparts osmotolerance on a strain of Lactobacillus acidophilus, Appl. Environ. Microbiol 53:2275-2281
  56. J$\ddot{o}$nsson, G., A. C. Midtvedt, A. Norman and T. Midtvedt. 1995, Intestinal microbial bile acid transformation in healthy infants, J. Pediatr. Gastroenterol. Nutr 20:394-402 https://doi.org/10.1097/00005176-199505000-00004
  57. Kempf, B. and E. Bremer. 1998, Uptake and synthesis of compatible solutes as microbial stress responses to highosmolality environments, Arch. Microbiol 170:319-330 https://doi.org/10.1007/s002030050649
  58. Kettunen, H., S. Peuranen, H. Jatila, P. Nurminen, M. Saarinen and J. Apajalahti. 1999, Effect of betaine on the microbiology of the chicken gastrointestinal tract. Proceedings of the 12th European Symposium on Poultry Nutrition. World's Poultry Science Association, Dutch Branch. Veldhoven, The Netherlands. p. 186
  59. Kettunen H., S. Peuranen and K. Tiihonen. 2001a, Betaine aids in the osmoregulation of duodenal epithelium of broiler chicks, and affects the movement of water across the small intestinal epithelium in vitro, Comp. Biochem. Physiol 129A:595-603
  60. Kettunen, H., K. Tiihonen, S. Peuranen, M. T. Saarinen and J. C. Remus. 2001b, Dietary betaine accumulates in the liver and intestinal tissue and stabilizes the intestinal epithelial structure in healthy and coccidia-infected broiler chicks, Comp. Biochem. Physiol 130A:759-769
  61. Kidd, M. T., P. R. Ferket and J. D. Garlich. 1997, Nutritional and osmoregulatory functions of betaine, World's Poult. Sci. J 53:125-139 https://doi.org/10.1079/WPS19970013
  62. Klasing, K. C., K. L. Adler, J. C. Remus and C. C. Calvert. 2002, Dietary betaine increases intraepithelial lymphocytes in the duodenum of coccidia-infected chicks and increases functional properties of phagocytes, J. Nutr 132:2274-2282
  63. Krishnan, S., B. S. Ramakrishna and H. J. Binder. 1999, Stimulation of sodium chloride absorption from secreting rat colon by short-chain fatty acids, Diges. Dis. Sci 44:1924-1930 https://doi.org/10.1023/A:1018871412748
  64. Landfald, B. and A. R. Strom. 1986, Choline-glycine betaine pathway confers a high level of osmotic tolerance in Escherichia coli, J. Bacteriol 165:849-855 https://doi.org/10.1016/0378-1097(86)90064-9
  65. Law, R. O. and M. B. Burg. 1991, The role of organic osmolytes in the regulation of mammalian cell volume. In: Advances of Comparative and Environmental Physiology, Vol. 9. Volume and Osmolality Control in Animal Cells (Ed. R. Gilles, E. K. Hoffmann and L. Bolis). Springer Verlag, New York. pp. 189- 225
  66. Lawrence, B. V., A. P. Schinckel, O. Adeola and K. Cera. 2002, Impact of betaine on pig finishing performance and carcass composition, J. Anim. Sci 80:475-482
  67. Le Rudulier, D. and L. Bouillard. 1983, Glycine betaine, an osmotic effector in Klebsiella pneumoniae and other members of the Enterobacteriaceae, Appl. Environ. Microbiol 46:152-159
  68. Lewis, A. J. 2003, Methionine-cystine relationships in pig nutrition. In: Amino acids in animal nutrition (Ed. J. P. F. D'Mello). CABI Publishing, Wallingford, Oxon, UK. pp. 143-155
  69. Lowry, K. R., O. A. Izquierdo and D. H. Baker. 1987, Efficacy of betaine relative to choline as a dietary methyl donor, Poult. Sci 66:135(Abstr.)
  70. Lu, J. J. and X. T. Zou. 2006, Effects of adding betaine on laying performance and contents of serum yolk precursors VLDL and VTG in laying hen. J. Zhejiang Univ. (Agric. Life Sci)32:287-291
  71. Matthews, J. O. and L. L. Southern. 2000, The effect of dietary betaine in Eimeria acervulina-infected chicks, Poult. Sci79:60-65
  72. Matthews J. O., L. L. Southern, T. D. Bidner and M. A. Persica. 2001a, Effects of betaine, pen space, and slaughter handling method on growth performance, carcass traits, and pork quality of finishing barrows, J. Anim. Sci 79:967-974
  73. Matthews, J. O., L. L. Southern and T. D. Bidner. 2001b, Estimation of the total sulfur amino acid requirement and the effect of betaine in diets deficient in total sulfur amino acids for the weanling pig, J. Anim. Sci 79:1557-1565
  74. Matthews, J. O., L. L. Southern, A. D. Higbie, M. A. Persica and T. D. Bidner. 2001c, Effects of betaine on growth, carcass characteristics, pork quality, and plasma metabolites of finishing pigs, J. Anim. Sci 79:722-728
  75. Matthews, J. O., L. L. Southern, J. E. Pontif, A. D. Higbie and T. D. Bidner. 1998, Interactive effects of betaine, crude protein, and net energy in finishing pigs, J. Anim. Sci. 76:2444-2455
  76. Matthews, J. O., T. L. Ward and L. L. Southern. 1997, Interactive effects of betaine and monensin in uninfected and Eimeria acervulina-infected chicks, Poult. Sci 76:1014-1019 https://doi.org/10.1007/s00265-008-0622-4.K.
  77. McDevitt, R. M., S. Mack and I. R. Wallis. 2000, Can betaine partially replace or enhance the effect of methionine by improving broiler growth and carcase characteristics? Br. Poult.Sci 41:473-480 https://doi.org/10.1080/713654957
  78. Mongin, P. 1976, Ionic constituents and osmolality of the small intestinal fluids of the laying hen, Br. Poult. Sci 17:383-392 https://doi.org/10.1080/00071667608416292
  79. Mosenthin, R., M. Eklund and A. Ratriyanto. 2007, Effects of betaine on ileal and faecal digestibilities and intestinal microbial fermentation of crude fibre in piglets. In:Manipulating pig production XI. (Eds. J. E. Paterson and J. A. Barker), Australasian Pig Science Association, Scott Print, Perth, Western Australia. p. 187
  80. NRC, National Research Council. 1994, Nutrient requirements of poultry, 9th ed. National Academic Press, Washington DC, US
  81. NRC, National Research Council. 1998, Nutrient requirements of swine. 10th ed, National Academic Press, Washington DC, US
  82. Noll, S. L., V. Stangeland, G. Speers, J. Brannon and J. Kalbfleisch. 2002, Betaine and breast meat yield in turkeys, Proc. Multistate Poultry Nutrition and Feeding Conf., Indianapolis, IN. Universities of Kentucky, Illinois, Michigan State, Purdue and Ohio State Cooperating. (http://ag.ansc.purdue.edu/ poultry/multistate/publication.htm)
  83. $\phi$verland, M., K. A. R$\phi$rvik and A. Skrede. 1999, Effect of trimethylamine oxide and betaine in swine diets on growth performance, carcass characteristics, nutrient digestibility, and sensory quality of pork, J. Anim. Sci 77:2143-2153
  84. Park, J. H., C. W. Kang and K. S. Ryu. 2006, Effects of feeding betaine on performance and blood hormone in laying hens, Korean J. Poult. Sci 33:323-328
  85. Perroud, B. and D. Le Rudulier. 1985, Glycine betaine transport in Escherichia coli: Osmotic modulation, J. Bacteriol 161:393-401
  86. Pesti, G. M., A. E. Harper and M. L. Sunde. 1979, Sulfur amino acid and methyl donor status of corn-soy diets fed to starting broiler chicks and turkey poults, Poult. Sci 58:1541-1547 https://doi.org/10.1590/S1516-635X2007000100008
  87. Petronini, P. G., E. M. De Angelis, P. Borghetti, A. F. Borghetti and K. P. Wheeler. 1992, Modulation by betaine of cellular responses to osmotic stress, Biochem. J 282:69-73 https://doi.org/10.1016/S0040-8166(95)80020-4
  88. Pettey, L. A., G. L. Cromwell, M. D. Lindemann, J. H. Randolph, H. J. Monegue, K. M. Laurent, G. R. Parker and R. D. Coffey. 2001, Efficacy of betaine as a carcass modifier in finishing pigs fed normal and low protein diets supplemented with amino acids, J. Anim. Sci 79(Suppl. 1):183(Abstr.)
  89. Pichereau, V., S. Bourot, S. Flahaut, C. Blanco, Y. Auffray and T. Bernard. 1999, The osmoprotectant glycine betaine inhibits salt-induced cross-tolerance towards lethal treatment in Enterococcus faecalis, Microbiol 145:427-435 https://doi.org/10.1099/13500872-145-2-427
  90. Pillai, P. B., A. C. Fanatico, K. W. Beers, M. E. Blair and J. L. Emmert. 2006, Homocysteine remethylation in young broilers fed varying levels of methionine, choline, and betaine, Poult. Sci. 85:90-95
  91. Pirompud, P., S. Attamangkune, C. Bunchasak and A. Promboon. 2005, Effect of feeding betaine to broilers reared under tropical conditions on performance and carcass traits. Proceedings of 43rd Kasetsart University Annual Conference, Thailand. p.254(Abstr.)
  92. Ratriyanto, A., M. Eklund and R. Mosenthin. 2007a, Effects of betaine supplementation on ileal and fecal digestibilities and intestinal microbial fermentation of nutrients in piglets, Proceedings International Scientific Symposium on Physiology of Livestock. Lithuanian Veterinary Academy, Kaunas, Lithuania. pp. 34-35
  93. Ratriyanto, A., R. Mosenthin and M. Eklund. 2007b, Effect of graded levels of dietary betaine on ileal and total tract digestibilities and intestinal microbial fermentation in piglets. Proceedings 119th VDLUFA Congress, G$\ddot{o}$ttingen, VDLUFAVerlag, Darmstadt, Germany. p. 87
  94. Remus, J. 2001, Betaine for increased breast meat yield in turkeys, World Poult 17:14-15
  95. Remus, J. C. and C. L. Quarles. 2000, The effect of betaine on lesion scores and tensile strength of coccidian-challenged broilers, Poult. Sci 79(Suppl. 1):118(Abstr.)
  96. Remus, J., E. Virtanen, L. Rosi and J. McNaughton. 1995, Effect of betaine on nutrient utilization of 21-day-old broilers during coccidiosis, Proceedings of the 10th European Symposium on Poultry Nutrition. World's Poultry Science Association, Turkish Branch, Antalya. Turkey. pp. 371-372
  97. R$\phi$rvik, K. A., S. H. Steien, B. Saltkjelsvik and M. S. Thomassen. 2000, Urea and trimethylamine oxide in diets for seawater farmed rainbow trout: Effect on fat belching, skin vesicle, winter ulcer and quality grading. Aquaculture Nutr 6:247-254 https://doi.org/10.1046/j.1365-2095.2000.00143.x
  98. Ryu, M. S., K. H. Cho, W. J. Shin and K. S. Ryu. 2002, Influence of dietary supplemental betaine on performance and egg quality of laying hens during the heat stress, Korean J. Poult.Sci 29:117-123
  99. Saarinen, M. T., H. Kettunen, K. Pulliainen, S. Peuranen, K. Tiihonen and J. Remus. 2001, A novel method to analyze betaine in chicken liver: Effect of dietary betaine and choline supplementation on the hepatic betaine concentration in broiler chicks, J. Agric. Food Chem 49:559-563 https://doi.org/10.1021/jf000675l
  100. Saunderson, C. L. and J. MacKinlay. 1990, Changes in bodyweight, composition and hepatic enzyme activities in response to dietary methionine, betaine and choline levels in growing chicks, Br. J. Nutr 63:339-349 https://doi.org/10.1079/BJN19900120
  101. Schrama, J. W., M. J. W. Heetkamp, P. H. Simmins and W. J. J. Gerrits. 2003, Dietary betaine supplementation affects energy metabolism of pigs, J. Anim. Sci 81:1202-1209
  102. Schutte, J. B., J. De Jong, W. Smink and M. Pack. 1997, Replacement value of betaine for DL-methionine in male broiler chicks, Poult. Sci 76:321-325
  103. Siljander-Rasi, H., S. Peuranen, K. Tiihonen, E. Virtanen, H. Kettunen, T. Alaviuhkola and P. H. Simmins. 2003, Effect of equi-molar dietary betaine and choline addition on performance, carcass quality and physiological parameters of pigs, Anim. Sci 76:55-62 https://doi.org/10.1016/j.cbpb.2003.09.015
  104. Simon, J. 1999, Choline, betaine and methionine interactions in chickens, pigs and fish (including crustaceans), World's Poult. Sci. J 55:353-374 https://doi.org/10.1079/WPS19990025
  105. Skomial, J. and M. Gagucki. 2003, Influence of supplemental betaine and B group vitamins in mixtures with different level of methionine on lipid metabolism in growing-finishing pigs, Ann. Anim. Sci 3 (Suppl. 2):139-143
  106. Smith, J. W. II, K. Q. Owen, J. L. Nelssen, R. D. Goodband, M. D. Tokach, K. G. Friesen, T. L. Lohrmann and S. A. Blum. 1994, The effect of dietary carnitine, betaine, and chromium nicotinate supplementation on growth and carcass characteristics in growing-finishing pigs, J. Anim. Sci 72(Suppl. 1):274(Abstr.)
  107. Smith, J. W. II, J. L. Nelssen, R. D. Goodband, M. D. Tokach, B. T. Richert, K. Q. Owen, J. R. Bergstrom and S. A. Blum. 1995, The effect of supplementing growing-finishing swine diets with betaine and (or) choline on growth and carcass characteristics, J. Anim. Sci 73(Suppl. 1):83(Abstr.)
  108. Snoswell, A. M. and G. P. Xue. 1987, Methyl group metabolism in sheep, Comp. Biochem. Physiol 88B:383-394
  109. Spreeuwenberg, M. A. M. S., H. M. J. Van Hees and C. H. M. Smits. 2007, The effect of betaine supplementation on growth performance of piglets raised under sub-optimal management conditions. In: Manipulating pig production XI. (Eds. J. E. Paterson and J. A. Barker). Australasian Pig Science Association, Scott Print, Perth, Western Australia. p. 186
  110. Stryer, L. 1988, Biosynthesis of amino acids and heme, In: Biochemistry, 3rd Ed. WH Freeman and Company, New York.pp. 575-626
  111. Suster, D., B. J. Leury, R. H. King, M. Mottram and F. R. Dunshea. 2004, Interrelationships between porcine somatotropin (pST), betaine, and energy level on body composition and tissue distribution of finisher boars, Aust. J. Agric. Res 55:983-990 https://doi.org/10.1071/AR04029
  112. Teeter, R. G., J. C. Remus, T. Belay, M. Mooney, E. Virtanen and P. Augustine. 1999, The effects of betaine on water balance and performance in broilers reared under differing environmental conditions, Proceedings of the Australian Poultry Science Symposium Vol 11. (Ed. D.J. Farrel). University of Sydney, Sydney, Australia. p. 165
  113. Tiihonen, K., S. Peuranen, H. Siljander-Rasi and H. P. Simmins. 2001. The effect of equi-molar betaine and coline additions on liver, plasma and gut of pig. J. Anim. Sci 79(Suppl. 1):390- 391
  114. Tsiagbe, V. K., M. E. Cook, A. E. Harper and M. L. Sunde. 1987, Enhanced immune responses in broiler chicks fed methionine supplemented diets, Poult. Sci. 66:1147-1154 https://doi.org/10.1590/S1516-635X2007000400006
  115. Tyler, D. D. 1977, Transport and oxidation of choline by liver mitochondria, Biochem. J 166:571-581
  116. Urbanczyk, J. 1997, An attempt to decrease pig carcass fatness by nutritive factors, Krmiva 39:311-325
  117. Virtanen, E. and L. Rosi. 1995, Effects of betaine on methionine requirement of broilers under various environmental conditions. Proceedings of the Australian Poultry Science Symposium Vol. 7. (Ed. D. Balnave), University of Sydney, Sydney, Australia. pp. 88-92
  118. Virtanen, E. and G. Rumsey. 1996, Betaine supplementation can optimize use of methionine, choline in diets, Feedstuffs 68:12-13
  119. Waldenstedt, L., K. Elwinger, P. Thebo and A. Uggla. 1999, Effect of betaine supplement on broiler performance during an experimental coccidial infection, Poult. Sci 78:182-189
  120. Waldroup, P. W., M. A. Motl, F. Yan and C. A. Fritts. 2006, Effects of betaine and choline on response to methionine supplementation to broiler diets formulated to industry standards, J. Appl. Poult. Res 15:58-71
  121. Wallis, I. R. 1999, Dietary supplements of methionine increase breast meat yield and decrease abdominal fat in growing broiler chickens, Aust. J. Exp. Agric 39:131-141 https://doi.org/10.1071/EA98130
  122. Wang, Y. Z. and Z. R. Xu. 1999, Effect of feeding betaine on weight gain and carcass trait of barrows and gilts and approach to mechanism, J. Zhejiang Agric. Univ. 25:281-285
  123. Wang, Y. Z., Z. R. Xu and J. Feng. 2004, The effect of betaine and DL-methionine on growth performance and carcass characteristics in meat ducks, Anim. Feed Sci. Technol 116:151-159 https://doi.org/10.1016/j.anifeedsci.2004.05.003
  124. Wenk, C., R. Kaliker and R. Messikommer. 1993, Whole maize plants in diets for growing pigs: effect of 3 different enzymes on the feed utilization. Proceedings of the 1st Symposium Enzymes in Animal Nutrition. (Ed. C. Wenk and M. Boessinger). Zurich, Switzerland. pp. 165-169
  125. Wray-Cahen, D., I. Fernández-Fígares, E. Virtanen, N. C. Steele and T. J. Caperna. 2004, Betaine improves growth, but does not induce whole body or hepatic palmitate oxidation in swine (Sus scrofa domestica), Comp. Biochem. Physiol. Part A 137:131-140
  126. Xing, W. and C. B. Rajashekar. 2001, Glycine betaine involvement in freezing tolerance and water stress in Arabidopsis thaliana, Environ. Exp. Bot 46:21-28 https://doi.org/10.1016/S0098-8472(01)00078-8
  127. Xu, Z. R. and D. Y. Yu. 2000, Effect of betaine on digestive function of weaned piglets, Chinese J. Vet. Sci 20:201-204
  128. Xu, Z. R. and X. A. Zhan. 1998, Effects of betaine on methionine and adipose metabolism in broiler chicks, Acta Vet. Zoot. Sinica 29:212-219
  129. Xue, G. P. and A. M. Snoswell. 1985, Comparative studies on the methionine synthesis in sheep and rat tissues, Comp. Biochem. Physiol, 80B:489-494
  130. Yamamoto, N., T. Tanaka and T. Noguchi. 1995, Effect of cysteine on expression of cystathionine beta-synthase in the rat liver, J. Nutr. Sci. Vitaminol 41:197-205 https://doi.org/10.3177/jnsv.41.197
  131. Yao, Z. and D. E. Vance. 1989, Head group specificity in the requirement of phosphatidylcholine biosynthesis for very low density lipoprotein secretion from cultured hepatocytes, J. Biol.Chem 264:11373-11380 https://doi.org/10.1096/fj.06-1005ufm
  132. Yu, D. Y., J. Feng and Z. R. Xu. 2001, Effects of betaine on fat and protein metabolism in different stages of swine, Chinese J. Vet. Sci 21:200-203
  133. Yu, D. Y., Z. R. Xu and W. F. Li. 2004, Effects of betaine on growth performance and carcass characteristics in growing pigs, Asian-Aust. J. Anim. Sci 17:1700-1704
  134. Yu, D. Y. and Z. R. Xu. 2000, Effect of methyl-donor on the performance and the mechanisms of growth-promoting hormone in piglets, Chinese J. Anim. Sci 36:8-10
  135. Zhan, X. A., J. X. Li, Z. R. Xu and R. Q. Zhao. 2006, Effects of methionine and betaine supplementation on growth performance, carcase composition and metabolism of lipids in male broilers, Br. Poult. Sci 47:576-580 https://doi.org/10.1080/00071660600963438
  136. Zhang, Z. and R. P. Wilson. 1999, Reevaluation of the choline requirement of fingerling channel catfish (Ictalurus punctatus) and determination of the availability of choline in common feed ingredients, Aquaculture 180:89-98 https://doi.org/10.1016/S0044-8486(99)00190-8
  137. Zou, X. T., Z. R. Xu and Y. Z. Wang. 2002, Effects of methylamino acids on growth performance of swine in different stages. J. Zhejiang Univ. (Agric. Life Sci.) 28:551-555
  138. Zou, X. T., Y. L. Ma and Z. R. Xu. 1998, Effects of betaine and thyroprotein on laying performance and approach to mechanism of the effects in hens, Acta Agric. Zhejiang.10:144-149
  139. Zulkifli, I., S. A. Mysahra and L. Z. Jin. 2004, Dietary supplementation of betaine (Betafin®) and response to high temperature stress in male broiler chickens, Asian-Aust. J. Anim. Sci 17:244-249

Cited by

  1. Plasma Lipids and Betaine Are Related in an Acute Coronary Syndrome Cohort vol.6, pp.7, 2011, https://doi.org/10.1371/journal.pone.0021666
  2. Plasma choline metabolites associate with metabolic stress among young overweight men in a genotype-specific manner vol.2, pp.10, 2012, https://doi.org/10.1038/nutd.2012.23
  3. Maternal dietary betaine supplementation modifies hepatic expression of cholesterol metabolic genes via epigenetic mechanisms in newborn piglets vol.112, pp.09, 2014, https://doi.org/10.1017/S0007114514002402
  4. Rendimentos de carcaça, cortes comerciais e não-componentes da carcaça de cordeiros Santa Inês alimentados com feno de erva-sal e concentrado vol.15, pp.1, 2014, https://doi.org/10.1590/S1519-99402014000100017
  5. Betaine Supplementation in Maternal Diet Modulates the Epigenetic Regulation of Hepatic Gluconeogenic Genes in Neonatal Piglets vol.9, pp.8, 2014, https://doi.org/10.1371/journal.pone.0105504
  6. In Ovo Injection of Betaine Affects Hepatic Cholesterol Metabolism through Epigenetic Gene Regulation in Newly Hatched Chicks vol.10, pp.4, 2015, https://doi.org/10.1371/journal.pone.0122643
  7. Betaine alleviates hepatic lipid accumulation via enhancing hepatic lipid export and fatty acid oxidation in rats fed with a high-fat diet vol.113, pp.12, 2015, https://doi.org/10.1017/S0007114515001130
  8. Effects of dietary betaine on growth performance, fat deposition and serum lipids in broilers subjected to chronic heat stress vol.86, pp.10, 2015, https://doi.org/10.1111/asj.12372
  9. Maternal betaine supplementation during gestation modifies hippocampal expression of GR and its regulatory miRNAs in neonatal piglets vol.78, pp.6, 2016, https://doi.org/10.1292/jvms.15-0678
  10. Effects of Dietary Protein Level and Betaine Supplementation on Nutrient Digestibility and Performance of Japanese Quails vol.19, pp.3, 2017, https://doi.org/10.1590/1806-9061-2016-0442
  11. H nuclear magnetic resonance (NMR)-based metabolomics pp.07307268, 2017, https://doi.org/10.1002/etc.3978
  12. Peculiarities of One-Carbon Metabolism in the Strict Carnivorous Cat and the Role in Feline Hepatic Lipidosis vol.5, pp.7, 2013, https://doi.org/10.3390/nu5072811
  13. Prospective associations of maternal betaine status with offspring weight and body composition at birth: the Growing Up in Singapore Towards healthy Outcomes (GUSTO) cohort study vol.104, pp.5, 2016, https://doi.org/10.3945/ajcn.116.138818
  14. Effects of feeding betaine-containing liquid supplement to transition dairy cows vol.100, pp.2, 2017, https://doi.org/10.3168/jds.2016-11452
  15. A new approach for separation and recovery of betaine from beet molasses based on cloud point extraction technique pp.0975-8402, 2018, https://doi.org/10.1007/s13197-017-2999-4
  16. Osmoregulatory function of betaine in alleviating heat stress in poultry pp.09312439, 2018, https://doi.org/10.1111/jpn.12990
  17. Bona fide choline monoxygenases evolved in Amaranthaceae plants from oxygenases of unknown function: Evidence from phylogenetics, homology modeling and docking studies vol.13, pp.9, 2018, https://doi.org/10.1371/journal.pone.0204711
  18. Betaine Improves Intestinal Functions by Enhancing Digestive Enzymes, Ameliorating Intestinal Morphology, and Enriching Intestinal Microbiota in High-salt stressed Rats vol.10, pp.7, 2018, https://doi.org/10.3390/nu10070907
  19. Whole-Transcriptome Sequence Analysis of Verbena bonariensis in Response to Drought Stress vol.19, pp.6, 2018, https://doi.org/10.3390/ijms19061751
  20. Betaine in Inflammation: Mechanistic Aspects and Applications vol.9, pp.1664-3224, 2018, https://doi.org/10.3389/fimmu.2018.01070
  21. Feed efficiency of diets with different energy and protein concentrations supplemented with methionine in laying quails vol.142, pp.1755-1315, 2018, https://doi.org/10.1088/1755-1315/142/1/012001
  22. Egg quality of quails fed low methionine diet supplemented with betaine vol.142, pp.1755-1315, 2018, https://doi.org/10.1088/1755-1315/142/1/012002
  23. Antimicrobial, cytotoxic and antioxidative evaluation of natural deep eutectic solvents vol.25, pp.14, 2018, https://doi.org/10.1007/s11356-018-1669-z
  24. A meta-analysis of the effects of dietary betaine supplementation on finishing performance and carcass characteristics of pigs vol.165, pp.1, 2009, https://doi.org/10.1016/j.anifeedsci.2011.02.008
  25. 베타인 사료의 급여시기가 폭염에 노출된 오리의 짧은 사슬지방산, 혈액 프로파일 및 생산성에 미치는 효과 vol.32, pp.3, 2009, https://doi.org/10.12925/jkocs.2015.32.3.427
  26. 폭염 하에서 음수 내 비타민 C와 트리메칠글리신 공급이 오리의 혈액 매개변수 및 생산성에 미치는 효과 vol.33, pp.3, 2016, https://doi.org/10.12925/jkocs.2016.33.3.411
  27. 폭염 하에서 음수 내 비타민 C와 트리메칠글리신 공급이 오리의 혈액 매개변수 및 생산성에 미치는 효과 vol.33, pp.3, 2016, https://doi.org/10.12925/jkocs.2016.33.3.411
  28. 사료 내 비테인 첨가 급여가 비육돈의 영양소 소화율 및 생리학적 변화에 미치는 영향 vol.17, pp.12, 2009, https://doi.org/10.5762/kais.2016.17.12.407
  29. Response of duck breeders to dietary L-Carnitine supplementation during summer season vol.91, pp.4, 2009, https://doi.org/10.1590/0001-3765201920180907
  30. Effects of Dietary Rumen-Protected Betaine Supplementation on Performance of Postpartum Dairy Cows and Immunity of Newborn Calves vol.9, pp.4, 2009, https://doi.org/10.3390/ani9040167
  31. Comparison of metabolomic responses of earthworms to sub-lethal imidacloprid exposure in contact and soil tests vol.26, pp.18, 2019, https://doi.org/10.1007/s11356-019-05302-y
  32. Influence of Early Heat Conditioning and Betaine or Ammonium Chloride Supplementation on Performance and Physiological Parameters of Quail Chicks in Hot Climate vol.18, pp.12, 2009, https://doi.org/10.3923/ijps.2019.562.569
  33. Dietary Betaine Addition Promotes Hepatic Cholesterol Synthesis, Bile Acid Conversion, and Export in Rats vol.12, pp.5, 2009, https://doi.org/10.3390/nu12051399
  34. Effects of rumen-protected folic acid and betaine supplementation on growth performance, nutrient digestion, rumen fermentation and blood metabolites in Angus bulls vol.123, pp.10, 2009, https://doi.org/10.1017/s0007114520000331
  35. Importance of Physiological Traits Vulnerability in Determine Halophytes Tolerance to Salinity Excess: A Comparative Assessment in Atriplex halimus vol.9, pp.6, 2009, https://doi.org/10.3390/plants9060690
  36. Effects of Dietary Rumen-Protected Betaine on Lactation Performance and Serum Metabolites of Mid-lactation Holstein Dairy Cows vol.68, pp.46, 2009, https://doi.org/10.1021/acs.jafc.9b07453
  37. Effect of betaine, a methyl group donor, on broiler chicken growth performance, breast muscle quality characteristics, oxidative status and amino acid content vol.19, pp.1, 2009, https://doi.org/10.1080/1828051x.2020.1773949
  38. Impact of Dietary Betaine and Metabolizable Energy Levels on Profiles of Proteins and Lipids, Bioenergetics, Peroxidation and Quality of Meat in Japanese Quail vol.11, pp.1, 2009, https://doi.org/10.3390/ani11010117
  39. Effects of dietary betaine on cholesterol metabolism and hepatopancreas function in gibel carp (Carassius gibelio) fed with a high‐fat diet vol.27, pp.6, 2009, https://doi.org/10.1111/anu.13316
  40. Dietary supplementation of betaine improves growth performance and reduces lipid peroxidation in Nile tilapia vol.27, pp.6, 2021, https://doi.org/10.1111/anu.13323
  41. Betaine and related compounds: Chemistry, metabolism and role in mitigating heat stress in poultry vol.104, pp.None, 2022, https://doi.org/10.1016/j.jtherbio.2021.103168