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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

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

Betaine;Methyl Group Donor;Osmolyte;Nutrient Digestibility

References

  1. 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
  2. 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
  3. 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
  4. 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
  5. 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.)
  6. 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
  7. 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
  8. 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.).
  9. Csonka, L. N. 1989, Physiological and genetic responses of bacteria to osmotic stress, Microbiol. Rev 53:121-147
  10. 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
  11. 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
  12. 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
  13. 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
  14. 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
  15. 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
  16. 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
  17. 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
  18. 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
  19. 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
  20. 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
  21. 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
  22. 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
  23. 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
  24. 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
  25. 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
  26. Matthews, J. O. and L. L. Southern. 2000, The effect of dietary betaine in Eimeria acervulina-infected chicks, Poult. Sci79:60-65
  27. 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
  28. 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
  29. 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
  30. Remus, J. 2001, Betaine for increased breast meat yield in turkeys, World Poult 17:14-15
  31. 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
  32. 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
  33. 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
  34. 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
  35. 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.)
  36. 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
  37. 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
  38. 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
  39. Virtanen, E. and G. Rumsey. 1996, Betaine supplementation can optimize use of methionine, choline in diets, Feedstuffs 68:12-13
  40. 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
  41. 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
  42. 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
  43. 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
  44. 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
  45. 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
  46. 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
  47. 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
  48. 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
  49. 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
  50. 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
  51. 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
  52. 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
  53. 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
  54. 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
  55. 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
  56. 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
  57. Stryer, L. 1988, Biosynthesis of amino acids and heme, In: Biochemistry, 3rd Ed. WH Freeman and Company, New York.pp. 575-626
  58. 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
  59. 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
  60. 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.)
  61. NRC, National Research Council. 1998, Nutrient requirements of swine. 10th ed, National Academic Press, Washington DC, US
  62. 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
  63. NRC, National Research Council. 1994, Nutrient requirements of poultry, 9th ed. National Academic Press, Washington DC, US
  64. 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
  65. Hochachka, P. W. and G. N. Somero. 1984, Biochemical Adaptation, Princeton University Press, Princeton, NJ, USA
  66. 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
  67. 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.)
  68. 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
  69. 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
  70. 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
  71. Xu, Z. R. and D. Y. Yu. 2000, Effect of betaine on digestive function of weaned piglets, Chinese J. Vet. Sci 20:201-204
  72. 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
  73. 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
  74. 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
  75. Urbanczyk, J. 1997, An attempt to decrease pig carcass fatness by nutritive factors, Krmiva 39:311-325
  76. 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
  77. 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
  78. 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
  79. 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
  80. 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
  81. 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
  82. 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
  83. 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
  84. 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
  85. 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
  86. 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)
  87. 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
  88. Perroud, B. and D. Le Rudulier. 1985, Glycine betaine transport in Escherichia coli: Osmotic modulation, J. Bacteriol 161:393-401
  89. 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.)
  90. 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
  91. 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
  92. 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
  93. 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
  94. Finkelstein, J. D. and J. J. Martin. 1984, Methionine metabolism in mammals. Distribution of homocysteine between competing pathways, J. Biol. Chem 259:9508-9513
  95. 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
  96. 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
  97. 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.)
  98. 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
  99. 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.)
  100. $\phi$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
  101. 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
  102. Glaasker, E., W. N. Konings and B. Poolman. 1996, Osmotic regulation of intracellular solute pools in Lactobacillus plantarum, J. Bacteriol 178:575-582
  103. 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
  104. Alaviuhkola, T. and K. Suomi. 1990, Effect of betaine supplementation of low methionine diet for growing pigs, Ann.Agric. Fenn 29:127-129
  105. 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
  106. 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
  107. 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
  108. 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
  109. 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.)
  110. 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
  111. 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
  112. 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
  113. 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
  114. 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
  115. 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
  116. 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
  117. 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
  118. 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
  119. 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.)
  120. 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
  121. 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
  122. Snoswell, A. M. and G. P. Xue. 1987, Methyl group metabolism in sheep, Comp. Biochem. Physiol 88B:383-394
  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. 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
  125. Finkelstein, J. D. and S. H. Mudd. 1967, Trans-sulfuration in mammals: The methionine-sparing effect of cystine, J. Biol.Chem 242:873-880
  126. 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
  127. 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
  128. 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
  129. 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
  130. Tyler, D. D. 1977, Transport and oxidation of choline by liver mitochondria, Biochem. J 166:571-581
  131. 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
  132. 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
  133. 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
  134. 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.
  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. 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
  137. 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
  138. 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
  139. 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

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