Dietary L-tryptophan supplementation with reduced large neutral amino acids enhances feed efficiency and decreases stress hormone secretion in nursery pigs under social-mixing stress

Journal of Nutrition

Volumn 142, Issue 8, 2012, Pages 1540-1546

  Shen, Yan Bin ^a   Voilquí, Gwendoline ^a   Odle, Jack ^a   Kim, Sung Woo ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 HYDROXYINDOLEACETIC ACID; AMINO ACID; HYDROCORTISONE; LARGE NEUTRAL AMINO ACID; MALONALDEHYDE; SEROTONIN; TRYPTOPHAN; UNCLASSIFIED DRUG;

5 HYDROXYINDOLEACETIC ACID BRAIN LEVEL; AGGRESSION; ANIMAL EXPERIMENT; ANIMAL FOOD; ARTICLE; BARROW (SWINE); BEHAVIOR; BLOOD SAMPLING; BODY WEIGHT; CONTROLLED STUDY; DIET SUPPLEMENTATION; DIETARY INTAKE; EXPERIMENTAL PIG; GROWTH CURVE; HORMONE RELEASE; HYPOTHALAMUS; NONHUMAN; PHYSICAL ACTIVITY; PRODUCTIVITY; SALIVA LEVEL; SEROTONIN BRAIN LEVEL; SOCIAL STRESS; UREA NITROGEN BLOOD LEVEL;

ADAPTATION, PHYSIOLOGICAL; AGGRESSION; AMINO ACIDS; ANIMAL FEED; ANIMALS; DIET; DIETARY SUPPLEMENTS; ENERGY METABOLISM; HYDROCORTISONE; HYPOTHALAMUS; MALE; MALONDIALDEHYDE; MOTOR ACTIVITY; SALIVA; SOCIAL BEHAVIOR; STRESS, PHYSIOLOGICAL; SWINE; TRYPTOPHAN;

SUIDAE;

EID: 84866281627     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.112.163824     Document Type: Article

References (68)

1. Ekkel ED, Savenije B, Schouten WG, Wiegant VM, Tielen MJ. The effects of mixing on behavior and circadian parameters of salivary cortisol in pigs. Physiol Behav. 1997;62:181-4.
2. Ruis MAW, te Brake JH, van de Burgwal JA, Jong IC, Blokhuis HJ, Koolhaas JM. Personalities in female domesticated pigs: behavioral and physiological indications. Appl Anim Behav Sci. 2000;66:31-47.
3. Jensen P, Yngvesson J. Aggression between unacquainted pigs: sequential assessment and effects of familiarity and weight. Appl Anim Behav Sci. 1998;58:49-61.
4. Guerra NG, Huesmann LR, Spindler A. Community violence exposure, social cognition, and aggression among urban elementary school children. Child Dev. 2003;74:1561-76.
5. Mason JW. A review of psychoendocrine research on the pituitaryadrenal cortical system. Psychosom Med. 1968;30 Suppl:576-607.
6. Henry JP, Meehan JP. Psychosocial stimuli, physiological specificity, and cardiovascular disease. Res Publ Assoc ResNervMent Dis. 1981;59:305-33.
7. Lepage O, Larson ET, Mayer I, Winberg S. Tryptophan affects both gastrointestinal melatonin production and interrenal activity in stressed and nonstressed rainbow trout. J Pineal Res. 2005;38:264-71.
8. Adeola O, Ball RO, House JD, O'Brien PJ. Regional brain neurotransmitter concentrations in stress-susceptible pigs. J Anim Sci. 1993;71:968-74.
9. Lepage O, Vilchez IM, Pottinger TG, Winberg S. Time-course of the effect of dietary L-tryptophan on plasma cortisol levels in rainbow trout Oncorhynchus mykiss. J Exp Biol. 2003;206:3589-99.
10. Koopmans SJ, Ruis M, Dekker R, van Diepen H, Korte M, Mroz Z. Surplus dietary tryptophan reduces plasma cortisol and noradrenaline concentrations and enhances recovery after social stress in pigs. Physiol Behav. 2005;85:469-78.
11. Cortamira NO, Seve B, Lebreton Y, Ganier P. Effect of dietary tryptophan on muscle, liver and whole-body protein synthesis in weaned piglets: relationship to plasma insulin. Br J Nutr. 1991;66:423-35.
12. Poletto R, Meisel RL, Richert BT, Cheng HW, Marchant-Forde JN. Aggression in replacement grower and finisher gilts fed a short-term high tryptophan diet and the effect of long-term human-animal interaction. Appl Anim Behav Sci. 2010;122:98-100.
13. Markus CR, Olivier B, Panhuysen GE, Van Der Gugten J, Alles MS, Tuiten A, Westenberg HG, Fekkes D, Koppeschaar HF, de Haan EE. The bovine protein alpha-lactalbumin increases the plasma ratio of tryptophan to the other large neutral amino acids, and in vulnerable subjects raises brain serotonin activity, reduces cortisol concentration, and improves mood under stress. Am J Clin Nutr. 2000;71:1536-44.
14. Zhang H, Yin J, Li D, Zhou X, Li X. Tryptophan enhances ghrelin expression and secretion associated with increased food intake and weight gain in weanling pigs. Domest Anim Endocrinol. 2007;33:47-61.
15. Fernstrom JD, Wurtman RJ. Brain serotonin content: physiological dependence on plasma tryptophan levels. Science. 1971;173:149-52.
16. Meunier-Salaün MC, Monnier M, Colleaux Y, Seve B, Henry Y. Impact of dietary tryptophan and behavioral type on behavior, plasma cortisol, and brain metabolites of young pigs. J Anim Sci. 1991;69:3689-98.
17. Attenburrow MJ, Williams C, Odontiadis J, Reed A, Powell J, Cowen PJ, Harmer CJ. Acute administration of nutritionally sourced tryptophan increases fear recognition. Psychopharmacology (Berl). 2003;169:104-7.
18. Koopmans SJ, Guzik AC, van derMeulen J, Dekker R, Kogut J, Kerr BJ, Southern LL. Effects of supplemental L-tryptophan on serotonin, cortisol, intestinal integrity, and behavior in weanling piglets. J Anim Sci. 2006;84:963-71.
19. Shen YB, Voilque G, Kim JD, Odle J, Kim SW. Effects of elevating tryptophan intake on growth and physiological changes in nursery pigs. J Anim Sci. Epub 2012 Jan 27.
20. Pardridge WM. CNS drug design based on principles of blood-brain barrier transport. J Neurochem. 1998;70:1781-92.
21. Fernstrom JD, Wurtman RJ. Brain serotonin content: physiological regulation by plasma neutral amino acids. Science. 1972;178:414-6.
22. Markus CR, Panhuysen G, Tuiten A, Koppeschaar H, Fekkes D, Peters ML. Does carbohydrate-rich, protein-poor food prevent a deterioration of mood and cognitive performance of stress-prone subjects when subjected to a stressful task? Appetite. 1998;31:49-65.
23. Scrutton H, Carbonnier A, Cowen PJ, Harmer CJ. Effects of alphalactalbumin on emotional processing in healthy women. J Psychopharmacol. 2007;21:519-24.
24. Markus CR, Verschoor E, Firk C, Kloek J, Gerhardt CC. Effect of tryptophan-rich egg protein hydrolysate on brain tryptophan availability, stress and performance. Clin Nutr. 2010;29:610-6.
25. Verschoor E, Finlayson G, Blundell J, Markus CR, King NA. Effects of an acute alpha-lactalbumin manipulation on mood and food hedonics in high- and low-trait anxiety individuals. Br J Nutr. 2010;104:595-602.
26. Lieberman HR, Wurtman JJ, Chew B. Changes in mood after carbohydrate consumption among obese individuals. Am J Clin Nutr. 1986;44:772-8.
27. NRC. Nutrient requirements of swine. 10th ed. Washington, DC: National Academic Press; 1998.
28. Kim SW, Wu G. Dietary arginine supplementation enhances the growth of milk-fed young pigs. J Nutr. 2004;134:625-30.
29. Wu G, Knabe DA, Kim SW. Arginine nutrition in neonatal pigs. J Nutr. 2004;134:S2783-90; discussion S96-7.
30. Mateo RD, Wu G, Bazer FW, Park JC, Shinzato I, Kim SW. Dietary L-arginine supplementation enhances the reproductive performance of gilts. J Nutr. 2007;137:652-6.
31. Adell A, Trullas R, Gelpi E. Time course of changes in serotonin and noradrenaline in rat brain after predictable or unpredictable shock. Brain Res. 1988;459:54-9.
32. Adell A, Garcia-Marquez C, Armario A, Gelpi E. Chronic stress increases serotonin and noradrenaline in rat brain and sensitizes their responses to a further acute stress. J Neurochem. 1988;50:1678-81.
33. Bethea CL, Lu NZ, Reddy A, Shlaes T, Streicher JM, Whittemore SR. Characterization of reproductive steroid receptors and response to estrogen in a rat serotonergic cell line. J Neurosci Methods. 2003;127:31-41.
34. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC. Measurement of protein using bicinchoninic acid. Anal Biochem. 1985;150:76-85.
35. Hicks TA, McGlone JJ, Whisnant CS, Kattesh HG, Norman RL. Behavioral, endocrine, immune, and performance measures for pigs exposed to acute stress. J Anim Sci. 1998;76:474-83.
36. Muqbil I, Banu N. Enhancement of pro-oxidant effect of 7,12-dimethylbenz (a) anthracene (DMBA) in rats by pre-exposure to restraint stress. Cancer Lett. 2006;240:213-20.
37. Zaidi SM, Al-Qirim TM, Banu N. Effects of antioxidant vitamins on glutathione depletion and lipid peroxidation induced by restraint stress in the rat liver. Drugs R D. 2005;6:157-65.
38. Katayama S, Mine Y. Antioxidative activity of amino acids on tissue oxidative stress in human intestinal epithelial cell model. J Agric Food Chem. 2007;55:8458-64.
39. Paredes SD, Bejarano I, Terron MP, Barriga C, Reiter RJ, Rodriguez AB. Melatonin and tryptophan counteract lipid peroxidation and modulate superoxide dismutase activity in ringdove heterophils in vivo. Effect of antigen-induced activation and age. Age (Dordr). 2009;31:179-88.
40. Tan DX, Manchester LC, Terron MP, Flores LJ, Reiter RJ. One molecule, many derivatives: a never-ending interaction of melatonin with reactive oxygen and nitrogen species? J Pineal Res. 2007;42:28-42.
41. Sampson EJ, Baird MA, Burtis CA, Smith EM, Witte DL, Bayse DD. A coupled-enzyme equilibrium method for measuring urea in serum: optimization and evaluation of the AACC study group on urea candidate reference method. Clin Chem. 1980;26:816-26.
42. Bolhuis JE, van den Brand H, Bartels AC, Oostindjer M, van den orne JJGC, Kemp B, Gerrits WJJ. Effects of fermentable starch on behaviour of growing pigs in barren or enriched housing. Appl Anim Behav Sci. 2010;123:77-86.
43. D'Eath RB. Individual aggressiveness measured in a resident-intruder test predicts the persistence of aggressive behavior and weight gain of young pigs after mixing. Appl Anim Behav Sci. 2002;77:267-83.
44. Li YZ, Kerr BJ, Kidd MT, Gonyou HW. Use of supplementary tryptophan to modify the behavior of pigs. J Anim Sci. 2006;84:212-20.
45. Rushen J. A difference in weight reduces fighting when unacquainted newly weaned pigs first meet. Can J Anim Sci. 1987;67:951-60.
46. Pérez-Cruet J, Chase TN, Murphy DL. Dietary regulation of brain tryptophan metabolism by plasma ratio of free tryptophan and neutral amino acids in humans. Nature. 1974;248:693-5.
47. Kaye WH, Gwirtsman HE, Brewerton TD, George DT, Wurtman RJ. Bingeing behavior and plasma amino acids: a possible involvement of brain serotonin in bulimia nervosa. Psychiatry Res. 1988;23:31-43.
48. Ashley DV, Liardon R, Leathwood PD. Breakfast meal composition influences plasma tryptophan to large neutral amino acid ratios of healthy lean young men. J Neural Transm. 1985;63:271-83.
49. Lambert GW, Kaye DM, Cox HS, Vaz M, Turner AG, Jennings GL, Esler MD. Regional 5-hydroxyindoleacetic acid production in humans. Life Sci. 1995;57:255-67.
50. Dinan TG. Serotonin: current understanding and the way forward. Int Clin Psychopharmacol. 1996;11 Suppl 1:19-21.
51. van Praag HM. Can stress cause depression? Prog Neuropsychopharmacol Biol Psychiatry. 2004;28:891-907.
52. Winberg S, Overli O, Lepage O. Suppression of aggression in rainbow trout (Oncorhynchus mykiss) by dietary L-tryptophan. J Exp Biol. 2001;204:3867-76.
53. Slag MF, Ahmad M, Gannon MC, Nuttall FQ. Meal stimulation of cortisol secretion: a protein induced effect. Metabolism. 1981;30:1104-8.
54. Gibson EL, Checkley S, Papadopoulos A, Poon L, Daley S, Wardle J. Increased salivary cortisol reliably induced by a protein-rich midday meal. Psychosom Med. 1999;61:214-24.
55. Chamberlain B, Ervin FR, Pihl RO, Young SN. The effect of raising or lowering tryptophan levels on aggression in vervet monkeys. Pharmacol Biochem Behav. 1987;28:503-10.
56. Eichelman BS. Neurochemical and psychopharmacologic aspects of aggressive behavior. Annu Rev Med. 1990;41:149-58.
57. Volavka J, Crowner M, Brizer D, Convit A, Van Praag H, Suckow RF. Tryptophan treatment of aggressive psychiatric inpatients. Biol Psychiatry. 1990;28:728-32.
58. Raleigh MJ, McGuire MT, Brammer GL, Pollack DB, Yuwiler A. Serotonergic mechanisms promote dominance acquisition in adult male vervet monkeys. Brain Res. 1991;559:181-90.
59. Shea MM, Mench JA, Thomas OP. The effect of dietary tryptophan on aggressive behavior in developing and mature broiler breeder males. Poult Sci. 1990;69:1664-9.
60. Sève B, Meunier-Salaun MC, Monnier M, Colleaux Y, Henry Y. Impact of dietary tryptophan and behavioral type on growth performance and plasma amino acids of young pigs. J Anim Sci. 1991;69:3679-88.
61. Insel TR, Roy BF, Cohen RM, Murphy DL. Possible development of the serotonin syndrome in man. Am J Psychiatry. 1982;139:954-5.
62. Hopkins TE, Wood CM, Walsh PJ. Interactions of cortisol and nitrogen metabolism in the ureogenic gulf toadfish Opsanus beta. J Exp Biol. 1995;198:2229-35.
63. McDonald MD, Wood CM. The effect of chronic cortisol elevation on urea metabolism and excretion in the rainbow trout (Oncorhynchus mykiss). J Comp Physiol B. 2004;174:71-81.
64. Tsopmo A, Diehl-Jones BW, Aluko RE, Kitts DD, Elisia I, Friel JK. Tryptophan released from mother's milk has antioxidant properties. Pediatr Res. 2009;66:614-8.
65. Peyrot F, Ducrocq C. Potential role of tryptophan derivatives in stress responses characterized by the generation of reactive oxygen and nitrogen species. J Pineal Res. 2008;45:235-46.
66. Christen S, Peterhans E, Stocker R. Antioxidant activities of some tryptophan metabolites: possible implication for inflammatory diseases. Proc Natl Acad Sci USA. 1990;87:2506-10.
67. Christen S, Thomas SR, Garner B, Stocker R. Inhibition by interferongamma of human mononuclear cell-mediated low density lipoprotein oxidation. Participation of tryptophan metabolism along the kynurenine pathway. J Clin Invest. 1994;93:2149-58.
68. Thomas SR, Witting PK, Stocker R. 3-Hydroxyanthranilic acid is an efficient, cell-derived co-antioxidant for alpha-tocopherol, inhibitingh human low density lipoprotein and plasma lipid peroxidation. J Biol Chem. 1996;271:32714-21.