Early social isolation alters behavioral and physiological responses to an endotoxin challenge in piglets

Hormones and Behavior

Volumn 50, Issue 5, 2006, Pages 753-761

  Tuchscherer, Margret ^a   Kanitz, Ellen ^a   Puppe, Birger ^a   Tuchscherer, Armin ^a  

^a LEIBNIZ INSTITUTE FOR FARM ANIMAL BIOLOGY FBN   (Germany)

Author keywords

Behavior; Hypothalamic pituitary adrenal axis; Immunity; Lipopolysaccharide; Sickness; Social isolation

Indexed keywords

CORTICOTROPIN; ENDOTOXIN; HYDROCORTISONE; LIPOPOLYSACCHARIDE; TRANSCORTIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; HORMONE RELEASE; ILLNESS BEHAVIOR; IMMUNE RESPONSE; NONHUMAN; PHYSIOLOGY; PRIORITY JOURNAL; SHIVERING; SOCIAL ISOLATION; SOMNOLENCE; STATISTICAL SIGNIFICANCE; SUCKLING; SWINE; VOMITING;

ADRENOCORTICOTROPIC HORMONE; ANIMALS; BEHAVIOR, ANIMAL; HYDROCORTISONE; IMMUNOGLOBULIN G; LIPOPOLYSACCHARIDES; MOTOR ACTIVITY; SHIVERING; SLEEP; SOCIAL ISOLATION; SUCKING BEHAVIOR; SWINE; TRANSCORTIN; TUMOR NECROSIS FACTOR-ALPHA; VOMITING;

EID: 33750949999     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2006.06.026     Document Type: Article

References (68)

1. Abraham E.J., Morris-Hardeman J.N., Swenson L.M., Knoppel E.L., Ramanathan B., Wright K.J., Grieger D.M., and Minton J.E. Pituitary function in the acute phase response in domestic farm animals: cytokines, prostaglandins, and secretion of ACTH. Dom. Anim. Endocrinol. 15 (1998) 389-396
2. Altmann J. Observational study of behavior: sampling methods. Behaviour 49 (1974) 227-267
3. Aubert A. Sickness and behaviour in animals: a motivational perspective. Neurosci. Biobehav. Rev. 23 (1999) 1029-1036
4. Avitsur R., Hunzeker J., and Sheridan J.F. Role of early stress in the individual differences in host response to viral infection. Brain Behav. Immun. 20 (2006) 339-348
5. Balaji R., Wright K.J., Turner J.L., Hill C.M., Dritz S.S., Fenwick B., Carroll J.A., Zanelli M.E., Beausang L.A., and Minton J.E. Circulating cortisol, tumor necrosis factor-α, interleukin-1β, and interferon-γ in pigs infected with Actinobacillus pleuropneumoniae. J. Anim. Sci. 80 (2002) 202-207
6. Barnard C.J., Behnke J.M., Gage A.R., Brown H., and Smithurst P.R. The role of parasite-induced immunodepression, rank and social environment in the modulation of behaviour and hormone concentration in male laboratory mice (Mus musculus). Proc. Biol. Sci. 265 (1998) 693-701
7. Baumann H., and Gauldie J. The acute phase response. Immunol. Today 15 (1994) 74-80
8. Becker B.A., and Misfeldt M.L. Evaluation of the mitogen-induced proliferation and cell surface differentiation antigens of lymphocytes from pigs 1 to 30 days of age. J. Anim. Sci. 71 (1993) 2073-2078
9. Beishuizen A., Thijs L.G., and Vermes I. Patterns of corticosteroid-binding globulin and the free cortisol index during septic shock and multitrauma. Intensive Care Med. 27 (2001) 1584-1591
10. Breuner C.W., and Orchinik M. Beyond carrier proteins. Plasma binding proteins as mediators of corticosteroid action in vertebrates. J. Endocrinol. 175 (2002) 99-112
11. Buwalda B., Felszeghy K., Horvath K.M., Nyakas C., de Boer S.F., Bohus B., and Koolhaas J.M. Temporal and spatial dynamics of corticosteroid receptor down-regulation in rat brain following social defeat. Physiol. Behav. 72 (2001) 349-354
12. Carobrez S.G., Gasparotto O.C., Buwalda B., and Bohus B. Long-term consequences of social stress on corticosterone and IL-1beta levels in endotoxin-challenged rats. Physiol. Behav. 76 (2002) 99-105
13. Dantzer R. Cytokine-induced sickness behavior: where do we stand?. Brain Behav. Immun. 15 (2001) 7-24
14. Dantzer R. Cytokine-induced sickness behaviour: a neuroimmune response to activation of innate immunity. Eur. J. Pharmacol. 500 (2004) 399-411
15. Dantzer R., Bluthé R.-M., Layé S., Bret-Dibat J.L., Parnet P., and Kelley K.W. Cytokines and sickness behavior. Ann. N. Y. Acad. Sci. 840 (1998) 586-590
16. De Groot J., Kruijt L., Scholten J.W., Boersma W.J.A., Buist W.G., Engel B., and van Reenen C.G. Age, gender and litter-related variation in T-lymphocyte cytokine production in young pigs. Immunology 115 (2005) 495-505
17. De La Garza R. Endotoxin- or pro-inflammatory cytokine-induced sickness behavior as an animal model of depression: focus on anhedonia. Neurosci. Biobehav. Rev. 29 (2005) 761-770
18. Fleshner M., Deak T., Spencer R.L., Laudenslager M.L., Watkins L.R., and Maier S.F. A long-term increase in basal levels of corticosterone and a decrease in corticosteroid-binding globulin after acute stressor exposure. Endocrinology 136 (1995) 5336-5342
19. Fraifeld V., and Kaplanski J. Brain eicosanoids and LPS fever: species and age differences. Prog. Brain Res. 115 (1998) 141-157
20. Fraser D. A review of the behavioural mechanism of milk ejection of the domestic pig. Appl. Anim. Ethol. 6 (1980) 247-255
21. Gaskins H.R. Immunological development and mucosal defence in the pig intestine. In: Wiseman J., Varley M.A., and Chadwick J.P. (Eds). Progress in Pig Science (1998), Nottingham Univ. Press, Nottingham 81-102
22. Gregory N.G. Physiological mechanisms causing sickness behaviour and suffering in diseased animals. Anim. Welf. 7 (1998) 293-305
23. Hammerberg C., Schurig G.G., and Ochs D.L. Immunodeficiency in young pigs. Am. J. Vet. Res. 50 (1989) 868-874
24. Hart B.L. Biological basis of the behavior of sick animals. Neurosci. Biobehav. Rev. 12 (1988) 123-137
25. Heim C., Owens M.J., Plotsky P.M., and Nemeroff C.B. Persistent changes in corticotropin-releasing factor systems due to early life experience: relationship to the pathophysiology of major depression and post-traumatic stress disorder. Psychopharmacol. Bull. 33 (1997) 185-192
26. Heim C., Newport D.J., Wagner D., Wilcox M.M., Miller A.H., and Nemeroff C.B. The role of early adverse experience and adulthood stress in the prediction of neuroendocrine stress reactivtiy in women: a multiple regression analysis. Depress. Anxiety 15 (2002) 117-125
27. Hennessy M.B., and Morris A. Passive response of young guinea pigs during exposure to a novel environment: influences of social partners and age. Dev. Psychobiol. 46 (2005) 86-96
28. Hennessy M.B., Deak T., and Schiml-Webb P.A. Stress-induced sickness behaviors: an alternative hypothesis for responses during maternal separation. Dev. Psychobiol. 39 (2001) 76-83
29. Heo J., Kattesh H.G., Roberts M.P., Morrow J.L., Dailey J.W., and Saxton A.M. Hepatic corticosteroid-binding globulin (CBG) messenger RNA expression and plasma CBG concentrations in young pigs in response to heat and social stress. J. Anim. Sci. 83 (2005) 208-215
30. Herskin M.S., and Jensen K.H. Effects of different degrees of social isolation on the behaviour of weaned piglets kept for experimental purposes. Anim. Welfare 9 (2000) 237-249
31. Hofer M.A. On the nature and consequences of early loss. Psychosom. Med. 58 (1996) 570-581
32. Huot R.L., Thrivikraman K.V., Menaey M.J., and Plotsky P.M. Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment. Psychopharmacology 158 (2001) 366-373
33. Johnson R.W. The concept of sickness behavior: a brief chronological account of four key discoveries. Vet. Immunol. Immunopathol. 87 (2002) 443-450
34. Johnson R.W., and von Borell E. Lipopolysaccharide-induced sickness behavior in pigs is inhibited by pretreatment with indomethacin. J. Anim. Sci. 72 (1994) 309-314
35. Johnson R.W., Propes M.J., and Shavit Y. Corticosterone modulates behavioral and metabolic effects of lipopolysaccharide. Am. J. Physiol. 270 (1996) R192-R198
36. Johnson J.D., O'Connor K.A., Deak T., Stark M., Watkins L.R., and Maier S.F. Prior stressor exposure sensitizes LPS-induced cytokine production. Brain. Behav. Immun. 16 (2002) 461-476
37. Kanitz E., Tuchscherer M., Tuchscherer A., Stabenow B., and Manteuffel G. Neuroendocrine and immune responses to acute endotoxemia in suckling and weaned piglets. Biol. Neonate 81 (2002) 203-209
38. Kanitz E., Tuchscherer M., Puppe B., Tuchscherer A., and Stabenow B. Consequences of repeated early isolation in domestic piglets (Sus scrofa) on their behavioural, neuroendocrine, and immunological responses. Brain Behav. Immun. 18 (2004) 35-45
39. Kattesh H.G., Charles S.F., Baumbach G.A., and Gillespie B.E. Plasma cortisol distribution in the pig from birth to six weeks of age. Biol. Neonate 58 (1990) 220-226
40. Kelley K.W., Johnson R.W., and Dantzer R. Immunology discovers physiology. Vet. Immunol. Immunopathol. 43 (1994) 157-165
41. Kelley K.W., Bluthé R.-M., Dantzer R., Zhou J.H., Shen W.H., Johnson R.W., and Broussard S.R. Cytokine-induced sickness behavior. Brain Behav. Immun. 17 (2003) 112-118
42. Klir J.J., Shahbazian L.M., Matteri R.L., Fritsche K.L., and Becker B.A. Effects of thermal environment on response to acute peripheral lipopolysaccharide challenge exposure in neonatal pigs. Am. J. Vet. Res. 58 (1997) 364-369
43. Krueger J.M., Majde J.A., and Obal F. Sleep in host defense. Brain Behav. Immun. 17 (2003) 41-47
44. Laban O., Marković B.M., Dimitrijević M., and Janković B.D. Maternal deprivation and early weaning modulate experimental allergic encephalomyelitis in the rat. Brain Behav. Immun. 9 (1995) 9-19
45. Ladd C.O., Huot R.L., Thrivikraman K.V., Nemeroff C.B., Meaney M.J., and Plotsky P.M. Long-term behavioural and neuroendocrine adaptations to adverse early experience. Prog. Brain Res. 122 (2000) 81-103
46. Larson S.J., and Dunn A.J. Behavioral effects of cytokines. Brain Behav. Immun. 15 (2001) 371-387
47. Liu D., Caldji C., Sharma S., Plotsky P.M., and Meaney M.J. Influence of neonatal rearing conditions on stress-induced adrenocorticotropin responses and norepinepherine release in the hypothalamic paraventricular nucleus. J. Neuroendocrinol. 12 (2000) 5-12
48. Maier S.F., and Wakins L.R. Cytokines for psychologists: implications of bi-directional immune-to-brain communication for understanding behavior, mood, and cognition. Psychol. Rev. 105 (1998) 83-107
49. Matteri R.L., Klir J.J., Fink B.N., and Johnson R.W. Neuroendocrine-immune interactions in the neonate. Dom. Anim. Endocrinol. 15 (1998) 397-407
50. Meaney M.J., Sapolsky R.M., and McEwen B.S. The development of the glucocorticoid receptor system in the rat limbic brain: I. Ontogeny and autoregulation. Brain Res. 350 (1985) 159-164
51. Milde A.M., Enger O., and Murison R. The effects of postnatal maternal separation on stress responsivity and experimentally induced colitis in adult rats. Physiol. Behav. 81 (2004) 71-84
52. Morrow-Tesch J., McGlone J.J., and Salak-Johnson J.L. Heat and social stress effects on pig immune measures. J. Anim. Sci. 72 (1994) 2599-2609
53. Owen-Ashley N.T., Turner M., Hahn T.P., and Wingfield J.C. Hormonal, behavioral, and thermoregulation responses to bacterial lipopolysaccharide in captive and free-living white-crowned sparrows (Zonotrichia leucophrys gambelii). Horm. Behav. 49 (2006) 15-29
54. Plotsky P.M., and Meaney M.J. Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Mol. Brain Res. 18 (1993) 195-200
55. Quan N., Avitsur R., Stark J.L., He L., Shah M., Caligiuri M., Padgett D.A., Marucha P.T., and Sheridan J.F. Social stress increases the susceptibility to endotoxic shock. J. Neuroimmunol. 115 (2001) 36-45
56. Sakumoto R., Kasuya E., Komatsu T., and Akita T. Central and peripheral concentrations of tumor necrosis factor-α in Chinese Meishan pigs stimulated with lipopolysaccharide. J. Anim. Sci. 81 (2003) 1274-1280
57. Salmon H. Immunité chez le foetus et le nouveau-né: modèle porcin. Reprod. Nutr. Dev. 24 (1984) 197-206
58. SAS Institute Inc. 2004. SAS/STAT® 9.1 User's Guide. Cary, NC: SAS Institute Inc.
59. Savu I., Zouaghi H., Carli A., and Nunez E.A. Serum depletion of corticosteroid binding activities, an early marker of human septic shock. Biochem. Biophys. Res. Commun. 102 (1981) 411-419
60. Schwager J., and Schulze J. Maturation of the mitogen responsiveness, and IL-2 and IL-6 production by neonatal swine leukocytes. Vet. Immunol. Immunopathol. 57 (1997) 105-119
61. Shanks N., Windle R.J., Perks P., Wood S., Ingram C.D., and Lightman S.L. The hypothalamic-pituitary-adrenal axis response to endotoxin is attenuated during lactation. J. Neuroendocrinol. 11 (1999) 857-865
62. Teunis M.A., Heijnen C.J., Sluyter F., Bakker J.M., Van Dam A.M., Hof M., Cools A.R., and Kavelaars A. Maternal deprivation of rat pups increases clinical symptoms of experimental autoimmune encephalomyelitis at adult age. J. Neuroimmunol. 133 (2002) 30-38
63. Tilders F.J.H., and Schmidt E.D. Cross-sensitization between immune and non-immune stressors. In: Dantzer R. (Ed). Cytokines, Stress, and Depression (1999), Plenum Publishers, New York 179-197
64. Tilders F.J.H., DeRijk R.H., Van Dam A.M., Vincent V.A.M., Schotanus K., and Persoons J.H.A. Activation of the hypothalamus-pituitary-adrenal axis by bacterial endotoxins: routes and intermediate signals. Psychoneuroendocrinology 19 (1994) 209-232
65. Tinnikov A.A. Responses of serum corticosterone and corticosteroid-binding globulin to acute and prolonged stress in the rat. Endocrine 11 (1999) 145-150
66. Tuchscherer M., Kanitz E., Puppe B., Tuchscherer A., and Stabenow B. Effects of postnatal social isolation on hormonal and immune responses of pigs to an acute endotoxin challenge. Physiol. Behav. 82 (2004) 503-511
67. Warren E.J., Finck B.N., Arkins S., Kelley K.W., Scamurra R.W., Murtaugh M.P., and Johnson R.W. Coincidental changes in behavior and plasma cortisol in unrestrained pigs after intracerebroventricular injection of tumor necrosis factor-α. Endocrinology 138 (1997) 2365-2371
68. Wright K.J., Balaji R., Hill C.M., Dritz S.S., Knoppel E.L., and Minton J.E. Integrated adrenal, somatotropic, and immune responses of growing pigs to treatment with lipopolysaccharide. J. Anim. Sci. 78 (2000) 1892-1899