Consequences of repeated early isolation in domestic piglets (Sus scrofa) on their behavioural, neuroendocrine, and immunological responses
Abstract
Stress in the form of intermittent maternal deprivation and social isolation during early postnatal life in rats and monkeys produces persistent changes in physiology and behaviour. In farm animals physiological consequences of disrupting mother-infant interactions with respect to health and animal welfare are relatively unknown. Therefore, the aim of the present study was to investigate the behavioural, neuroendocrine and immunological consequences of a 2 h daily social isolation from day 3 to day 11 of age in domestic piglets as well as potential long-term effects on the brain-endocrine-immune regulation. Repeated social isolation resulted in significantly decreased open-field activity (locomotion, vocalization) during the isolation period, increased basal cortisol concentrations and decreased lymphocyte proliferation in response to concanavalin A and pokeweed mitogen one day after the isolation. There was also a significant increase of interleukin-1beta (IL-1beta) concentration in hippocampus in isolated piglets compared to controls at this time. Six weeks after isolation significant enhanced basal ACTH concentrations as well as higher IL-1beta content and glucocorticoid receptor (GR) binding in hippocampus were found. These endocrine and immune responses were associated with decreased CRH levels in the hypothalamus and increased CRH content in the amygdala. The present data indicate that early social isolation in pigs may cause changes in behavioural, neuroendocrine, and immune regulation and produce long-term effects not only on the activity of the hypothalamic-pituitary-adrenal (HPA) system, but also on the immune-brain circuitry with possible negative consequences in health and welfare of commercial pigs. Using the pig as a suitable animal model, the finding of this study may also have some implications for the etiology of anxiety and depression in humans.
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Social isolation decreases open field activity, raises basal cortisol, and reduces lymphocyte proliferation to mitogens in pigs.
“decreases open field activity, increases in basal cortisol concentrations, and decreases in lymphocyte proliferation to mitogens in pigs;18”
From Social isolation (2011) · cites this paper as [18]
Cites
PROTEIN MEASUREMENT WITH THE FOLIN PHENOL REAGENT
Lowry, O. H., Rosebrough, N., Farr, A. L., & Randall, R. (1951) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)52451-6 · Cited by 315,771 · see citing works
THE ATTRACTIONS OF PROTEINS FOR SMALL MOLECULES AND IONS
Scatchard, G. (1949) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1949.tb27297.x · Cited by 19,724 · see citing works
Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P. M., & Meaney, M. J. (1997) · Science · doi:10.1126/science.277.5332.1659 · Cited by 3,170 · see citing works
The psychology of fear and stress
(1988) · Choice Reviews Online · doi:10.5860/choice.26-2399 · Cited by 3,134 · see citing works
Neurocircuitry of stress: central control of the hypothalamo–pituitary–adrenocortical axis
Herman, J. P., & Cullinan, W. E. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)10069-2 · Cited by 2,270 · see citing works
Plotsky, P. M., & Meaney, M. J. (1993) · Molecular Brain Research · doi:10.1016/0169-328x(93)90189-v · Cited by 1,638 · see citing works
Maier, S. F., & Watkins, L. R. (1998) · Psychological Review · doi:10.1037/0033-295x.105.1.83 · Cited by 1,130 · see citing works
Meaney, M. J., Diorio, J., Francis, D., Widdowson, J., LaPlante, P., Caldji, C., Sharma, S., Seckl, J. R., & Plotsky, P. M. (2010) · Developmental Neuroscience · doi:10.1159/000111395 · Cited by 878 · see citing works
Environmental Enrichment Reverses the Effects of Maternal Separation on Stress Reactivity
Francis, D. D., Diorio, J., Plotsky, P. M., & Meaney, M. J. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-18-07840.2002 · Cited by 663 · see citing works
Exposure to Acute Stress Induces Brain Interleukin-1β Protein in the Rat
Nguyen, K. T., Deak, T., Owens, S. M., Kohno, T., Fleshner, M., Watkins, L. R., & Maier, S. F. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-06-02239.1998 · Cited by 460 · see citing works
Levine, S. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00496-6 · Cited by 428 · see citing works
Makino, S., Gold, P. W., & Schulkin, J. (1994) · Brain Research · doi:10.1016/0006-8993(94)91862-7 · Cited by 400 · see citing works
Stress and the hypothalamo-pituitary-adrenal axis: acute, chronic and immunological activation
Harbuz, M. S., & Lightman, S. L. (1992) · Journal of Endocrinology · doi:10.1677/joe.0.1340327 · Cited by 334 · see citing works
Levine, S. D., Huchton, D. M., Wiener, S. G., & Rosenfeld, P. (1991) · Developmental Psychobiology · doi:10.1002/dev.420240803 · Cited by 304 · see citing works
Stress and immunity: A unifying concept
Griffin, J. F. T. (1989) · Veterinary Immunology and Immunopathology · doi:10.1016/0165-2427(89)90005-6 · Cited by 269 · see citing works
Albeck, D. S., McKittrick, C. R., Blanchard, D. C., Blanchard, R. J., Nikulina, J., McEwen, B. S., & Sakai, R. R. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-12-04895.1997 · Cited by 261 · see citing works
Immobilization stress induces interleukin-1β mRNA in the rat hypothalamus
Minami, M., Kuraishi, Y., Yamaguchi, T., Nakai, S., Hirai, Y., & Satoh, M. (1991) · Neuroscience Letters · doi:10.1016/0304-3940(91)90944-o · Cited by 258 · see citing works
Minton, J. E. (1994) · Journal of Animal Science · doi:10.2527/1994.7271891x · Cited by 252 · see citing works
Shintani, F., Nakaki, T., Kanba, S., Sato, K., Yagi, G., Shiozawa, M., Aiso, S., Kato, R., & Asai, M. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-03-01961.1995 · Cited by 245 · see citing works
Role of interleukin-1 beta in impairment of contextual fear conditioning caused by social isolation
Pugh, C. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(99)00098-4 · Cited by 244 · see citing works
Heat and social stress effects on pig immune measures1
Morrow-Tesch, J. L., McGlone, J. J., & Salak‐Johnson, J. L. (1994) · Journal of Animal Science · doi:10.2527/1994.72102599x · Cited by 227 · see citing works
Heim, C. C., Owens, M. J., Plotsky, P. M., & Nemeroff, C. B. (1997) · PubMed · Cited by 206 · see citing works
Matthews, K., Wilkinson, L. S., & Robbins, T. W. (1996) · Physiology & Behavior · doi:10.1016/0031-9384(95)02069-1 · Cited by 178 · see citing works
Maier, S. F., & Watkins, L. R. (1995) · Brain Research · doi:10.1016/0006-8993(95)00930-o · Cited by 178 · see citing works
McCormick, C. M., Kehoe, P., & Kovacs, S. (1998) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(98)00026-4 · Cited by 170 · see citing works
Makino, S., Shibasaki, T., Yamauchi, N., Nishioka, T., Mimoto, T., Wakabayashi, I., Gold, P. W., & Hashimoto, K. (1999) · Brain Research · doi:10.1016/s0006-8993(99)02114-9 · Cited by 168 · see citing works
On the nature and consequences of early loss
Hofer, M. A. (1996) · Psychosomatic Medicine · doi:10.1097/00006842-199611000-00005 · Cited by 152 · see citing works
Handbook of Squirrel Monkey Research
Rosenblum, L. A., & Coe, C. L. (1985) · Springer eBooks · doi:10.1007/978-1-4757-0812-7 · Cited by 147 · see citing works
Adaptation to social isolation
Ruis, M. A. W., Brake, J. H. A. T., ENGEL, B., Buist, W. G., Blokhuis, H. J., & Koolhaas, J. M. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00548-0 · Cited by 146 · see citing works
Psychosocial Stress and Urinary Cortisol Excretion in Marmoset Monkeys
SMITH, T., & French, J. A. (1997) · Physiology & Behavior · doi:10.1016/s0031-9384(97)00103-0 · Cited by 143 · see citing works
Effects of social status after mixing on immune, metabolic, and endocrine responses in pigs
Tuchscherer, M., Puppe, B., Tuchscherer, A., & Kanitz, E. (1998) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00084-5 · Cited by 134 · see citing works
Self-citationJensen, M. B., Vestergaard, K. S., Krohn, C. C., & Munksgaard, L. (1997) · Applied Animal Behaviour Science · doi:10.1016/s0168-1591(96)01183-5 · Cited by 130 · see citing works
Watts, A. G. (1996) · Frontiers in Neuroendocrinology · doi:10.1006/frne.1996.0008 · Cited by 130 · see citing works
Bhatnagar, S., & Meaney, M. J. (1995) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1995.tb00672.x · Cited by 127 · see citing works
Francis, D. D., Diorio, J. C., LaPlante, P., Weaver, S., Seckl, J. R., & Meaney, M. J. (1996) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1996.tb32517.x · Cited by 113 · see citing works
Effects of Early Rearing Environment on Immune-Responses of Infant Rhesus Monkeys
Lubach, G. R., Coe, C. L., & Ershler, W. B. (1995) · Brain Behavior and Immunity · doi:10.1006/brbi.1995.1004 · Cited by 107 · see citing works
The vocalizations and other behaviour of growing pigs in an “open field” test
Fraser, D. J. (1974) · Applied Animal Ethology · doi:10.1016/0304-3762(74)90003-0 · Cited by 99 · see citing works
Neuroendocrine integration of stress and significance of stress for the performance of farm animals
von Borell, E. (1995) · Applied Animal Behaviour Science · doi:10.1016/0168-1591(95)00615-y · Cited by 99 · see citing works
Early environmental programming hypothalamic-pituitary-adrenal responses to stress
Meaney, M. J., Tannenbaum, B. M., Francis, D. D., Bhatnagar, S., Shanks, N. M., Viau, V., O’Donnell, D., & Plotsky, P. M. (1994) · Seminars in Neuroscience · doi:10.1006/smns.1994.1032 · Cited by 96 · see citing works
Weiler, U., Claus, R., Combes, S., & Louveau, I. (1998) · Livestock Production Science · doi:10.1016/s0301-6226(97)00165-6 · Cited by 96 · see citing works
Relationship between behaviour and adrenocortical response pattern in domestic pigs
von Borell, E., & Ladewig, J. (1992) · Applied Animal Behaviour Science · doi:10.1016/s0168-1591(05)80115-7 · Cited by 88 · see citing works
Influence of early rearing on lymphocyte proliferation responses in juvenile rhesus monkeys
Coe, C. L., Lubach, G. R., Ershler, W. B., & Klopp, R. G. (1989) · Brain Behavior and Immunity · doi:10.1016/0889-1591(89)90005-6 · Cited by 87 · see citing works
Plata‐Saláman, C. R., Ilyin, S. E., Turrin, N. P., Gayle, D. A., Flynn, M. C., Bedard, T., Merali, Z., & Anisman, H. (2000) · Brain Research Bulletin · doi:10.1016/s0361-9230(99)00204-x · Cited by 84 · see citing works
Huber, K. M., Sawtell, N. B., & Bear, M. F. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-01-00001.1998 · Cited by 80 · see citing works
Mohammed, K., & Hubbard, J. P. (1983) · Endocrinology · doi:10.1210/endo-113-3-1161 · Cited by 73 · see citing works
Weaver, S., AHERNE, F. X., Meaney, M., Schaefer, A. L., & Dixon, W. T. (2000) · Journal of Endocrinology · doi:10.1677/joe.0.1640349 · Cited by 71 · see citing works
A general reaction pattern across situations in prepubertal gilts
Thodberg, K., Jensen, K. H., & Herskin, M. S. (1999) · Applied Animal Behaviour Science · doi:10.1016/s0168-1591(99)00009-x · Cited by 67 · see citing works
Hennessy, M. B., Terrence Deak, B., & Schiml‐Webb, P. A. (2001) · Developmental Psychobiology · doi:10.1002/dev.1031 · Cited by 66 · see citing works
Early Environmental Regulation of Glucocorticoid Feedback Sensitivity in Young Adult Monkeys
Lyons, D. M., Yang, C., Mobley, B. W., Nickerson, J., & Schatzberg, A. F. (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00505.x · Cited by 64 · see citing works
Often, W., Kanitz, E., Tuchscherer, M., & Nürnberg, G. (2001) · Animal Science · doi:10.1017/s1357729800058252 · Cited by 64 · see citing works
Self-citationImmunoradiometric assay of corticotropin with use of avidin-biotin separation.
Zahradnik, R. J., Brennan, G., Hutchison, J. S., & Odell, W. D. (1989) · Clinical Chemistry · doi:10.1093/clinchem/35.5.804 · Cited by 60 · see citing works
Neuroendocrine and Immune Responses to Acute Endotoxemia in Suckling and Weaned Piglets
Kanitz, E., Tuchscherer, M., Tuchscherer, A., Stabenow, B., & Manteuffel, G. (2002) · Neonatology · doi:10.1159/000051535 · Cited by 59 · see citing works
Self-citationHerskin, M. S., & Jensen, K. H. (2000) · Animal Welfare · doi:10.1017/s0962728600022727 · Cited by 58 · see citing works
Stress, the immune system, and psychiatry /
Leonard, B. E., & Miller, K. (1995) · Cited by 56 · see citing works
Social separation and reunion affects immune system in juvenile rhesus monkeys
Gordon, T. P., Gust, D. A., Wilson, M. E., Ahmed‐Ansari, A., Brodie, A. R., & McClure, H. M. (1992) · Physiology & Behavior · doi:10.1016/0031-9384(92)90166-y · Cited by 54 · see citing works
Juvenile Friends, Behavior, and Immune Responses to Separation in Bonnet Macaque Infants
Boccia, M. L., Scanlan, J. M., Laudenslager, M. L., Berger, C. L., Hijazi, A. S., & Reite, M. L. (1997) · Physiology & Behavior · doi:10.1016/s0031-9384(96)00370-8 · Cited by 53 · see citing works
Schrader, L., & Ladewig, J. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(99)00015-3 · Cited by 51 · see citing works
Kanitz, E., Manteuffel, G., & Otten, W. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00712-4 · Cited by 42 · see citing works
Self-citationInfluence of early life events on immune reactivity in adult mice
Neveu, P. J., Deleplanque, B., Puglisi‐Allegra, S., D'Amato, F. R., & Cabib, S. (1994) · Developmental Psychobiology · doi:10.1002/dev.420270403 · Cited by 40 · see citing works
Stress, the Immune System and Psychiatry
Krahn, L. E. (1996) · Mayo Clinic Proceedings · doi:10.4065/71.2.214-a · Cited by 39 · see citing works
Kanitz, E., Otten, W., Nürnberg, G., & Brüssow, K. ‐. (1999) · Animal Science · doi:10.1017/s1357729800050542 · Cited by 36 · see citing works
Self-citationPhysiological Consequences of Maternal Separation and Loss in the Squirrel Monkey
Coe, C. L., Wiener, S. G., Rosenberg, L. T., & Levine, S. D. (1985) · Springer eBooks · doi:10.1007/978-1-4757-0812-7_5 · Cited by 31 · see citing works
Molecular Mechanisms Underlying the Actions of the Pro-inflammatory Cytokine Interleukin I
O'Neill, L. A. J. (1997) · Biochemical Society Transactions · doi:10.1042/bst0250295 · Cited by 27 · see citing works
Yang, W., & Schultz, R. D. (1986) · Veterinary Immunology and Immunopathology · doi:10.1016/0165-2427(86)90045-0 · Cited by 24 · see citing works
Puppe, B., Schön, P. C., & Wendland, K. (1999) · Laboratory Animals · doi:10.1258/002367799780578110 · Cited by 24 · see citing works
Self-citationEffect of housing on open-field test behavior of gestating gilts
Taylor, L., & Friend, T. H. (1987) · Applied Animal Behaviour Science · doi:10.1016/0168-1591(87)90011-6 · Cited by 21 · see citing works
Open-field test behavior of growing swine maintained on a concrete floor and a pasture
Taylor, L., & Friend, T. H. (1986) · Applied Animal Behaviour Science · doi:10.1016/0168-1591(86)90106-1 · Cited by 19 · see citing works
Stress, the Hypothalamic-Pituitary-Adrenal Axis, and Immune Function
Stein, M., & Miller, A. H. (1993) · Advances in experimental medicine and biology · doi:10.1007/978-1-4615-2980-4_1 · Cited by 17 · see citing works
Psychoneuroimmunology of stress
Dantzer, R., & Mormède, P. (1995) · HAL (Le Centre pour la Communication Scientifique Directe) · Cited by 17 · see citing works
Lymphocyte protein synthesis: evidence that murine T cells are more affected by stress than B cells
Domínguez‐Gerpe, L., & Lefkovits, I. (1996) · Immunology Letters · doi:10.1016/0165-2478(96)02594-1 · Cited by 12 · see citing works
Regulation of pituitary peptides by the immune system
HALL, N. R. S., & O’Grady, M. P. (1989) · BioEssays · doi:10.1002/bies.950110507 · Cited by 8 · see citing works
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Cacioppo, J. T., & Hawkley, L. C. (2009) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2009.06.005 · Cited by 2,144 · see citing works
Social relationships and health: The toxic effects of perceived social isolation
Cacioppo, J. T., & Cacioppo, S. (2014) · Social and Personality Psychology Compass · doi:10.1111/spc3.12087 · Cited by 1,057 · see citing works
Sources of stress in captivity
Morgan, K. N., & Tromborg, C. T. (2007) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2006.05.032 · Cited by 1,085 · see citing works
Alone in the crowd: The structure and spread of loneliness in a large social network.
Cacioppo, J. T., Fowler, J. H., & Christakis, N. A. (2009) · Journal of Personality and Social Psychology · doi:10.1037/a0016076 · Cited by 844 · see citing works
Exploration of the hypothalamic–pituitary–adrenal function as a tool to evaluate animal welfare
Mormède, P., Andanson, S., Aupérin, B., Beerda, B., Guemene, D. D., Malmkvist, J., Manteca, X., Manteuffel, G., Prunet, P., van Reenen, C. G., et al. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.12.003 · Cited by 821 · see citing works
Evolutionary mechanisms for loneliness
Cacioppo, J. T., Cacioppo, S., & Boomsma, D. I. (2014) · Cognition and Emotion · doi:10.1080/02699931.2013.837379 · Cited by 576 · see citing works
Cacioppo, J. T., Hawkley, L. C., Norman, G. J., & Berntson, G. G. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2011.06028.x · Cited by 554 · see citing works
The use of pigs in neuroscience: Modeling brain disorders
Lind, N. M., Moustgaard, A., Jelsing, J., Vajta, G., Cumming, P. D., & Hansen, A. K. (2007) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.02.003 · Cited by 515 · see citing works
Effects of social isolation on glucocorticoid regulation in social mammals
Hawkley, L. C., Cole, S. W., Capitanio, J. P., Norman, G. J., & Cacioppo, J. T. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.05.011 · Cited by 262 · see citing works
Making sense of apparently conflicting data: Stress and immunity in swine and cattle1
Salak‐Johnson, J. L., & McGlone, J. J. (2007) · Journal of Animal Science · doi:10.2527/jas.2006-538 · Cited by 255 · see citing works
Cognitive enrichment affects behavioural reactivity in domestic pigs
Puppe, B., Ernst, K., Schön, P. C., & Manteuffel, G. (2006) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2006.05.016 · Cited by 166 · see citing works
Self-citationBirth practices: Maternal‐neonate separation as a source of toxic stress
Bergman, N. (2019) · Birth Defects Research · doi:10.1002/bdr2.1530 · Cited by 169 · see citing works
The Sacred Hour: Uninterrupted Skin-to-Skin Contact Immediately After Birth
Phillips, R. M. (2013) · Newborn and Infant Nursing Reviews · doi:10.1053/j.nainr.2013.04.001 · Cited by 138 · see citing works
Earley, R. L., Edwards, J. T., Aseem, S. O., Felton, K., Blumer, L. S., Karom, M. C., & Grober, M. S. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.04.002 · Cited by 135 · see citing works
The Importance of Early Experiences for Neuro-Affective Development
Tottenham, N. (2013) · Current topics in behavioral neurosciences · doi:10.1007/7854_2013_254 · Cited by 133 · see citing works
Effects of cognitive enrichment on behavioural and physiological reactions of pigs
Zebunke, M., Puppe, B., & Langbein, J. (2013) · Physiology & Behavior · doi:10.1016/j.physbeh.2013.05.005 · Cited by 130 · see citing works
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Proudfoot, K. L., & Habing, G. G. (2015) · The Veterinary Journal · doi:10.1016/j.tvjl.2015.05.024 · Cited by 133 · see citing works
The Importance of Early Experiences for Neuro-Affective Development
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Pathological anxiety in animals
Ohl, F., Arndt, S. S., & van der Staay, F. J. (2007) · The Veterinary Journal · doi:10.1016/j.tvjl.2006.12.013 · Cited by 125 · see citing works
A review of behavioural methods to study emotion and mood in pigs, Sus scrofa
Murphy, E., Nordquist, R. E., & van der Staay, F. J. (2014) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2014.08.002 · Cited by 123 · see citing works
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Moya, S. L., Boyle, L. A., Lynch, P. B., & Arkins, S. (2007) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2007.05.019 · Cited by 109 · see citing works
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Hostetler, C. M., & Ryabinin, A. E. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00092 · Cited by 105 · see citing works
Are Large Physiological Reactions to Acute Psychological Stress Always Bad for Health?
Carroll, D., Lovallo, W. R., & Phillips, A. C. (2009) · Social and Personality Psychology Compass · doi:10.1111/j.1751-9004.2009.00205.x · Cited by 106 · see citing works
Ellen, E. D., Rodenburg, T. B., Albers, G. A. A., Bolhuis, J. E., Camerlink, I., Duijvesteijn, N., Knol, E. F., Muir, W. M., Peeters, K., Reimert, I., et al. (2014) · Frontiers in Genetics · doi:10.3389/fgene.2014.00377 · Cited by 104 · see citing works
Bolt, S. L., Boyland, N. K., Mlynski, D. T., James, R., & Croft, D. P. (2017) · PLoS ONE · doi:10.1371/journal.pone.0166926 · Cited by 94 · see citing works
Poletto, R., Steibel, J. P., Siegford, J. M., & Zanella, A. J. (2006) · Brain Research · doi:10.1016/j.brainres.2005.10.001 · Cited by 86 · see citing works
Leslie, E. E. C., Hernández‐Jover, M., Newman, R. E., & Holyoake, P. (2010) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2010.09.006 · Cited by 87 · see citing works
Kanitz, E., Puppe, B., Tuchscherer, M., Heberer, M., Viergutz, T., & Tuchscherer, A. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.05.007 · Cited by 81 · see citing works
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Self-citationLeliveld, L. M. C., Düpjan, S., Tuchscherer, A., & Puppe, B. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.02.002 · Cited by 78 · see citing works
Self-citationEricsson, M., Henriksen, R., Bélteky, J., Sundman, A.-S., Shionoya, K., & Jensen, P. (2016) · PLoS ONE · doi:10.1371/journal.pone.0153879 · Cited by 73 · see citing works
Kranendonk, G., van der Mheen, H., Fillerup, M., & Hopster, H. (2007) · Journal of Animal Science · doi:10.2527/jas.2006-074 · Cited by 70 · see citing works
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Kick, A. R., Tompkins, M. B., Flowers, W. L., Whisnant, C. S., & Almond, G. W. (2011) · Journal of Animal Science · doi:10.2527/jas.2010-3470 · Cited by 69 · see citing works
Tuchscherer, M., Kanitz, E., Puppe, B., Tuchscherer, A., & Stabenow, B. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.04.056 · Cited by 66 · see citing works
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Briefer, E. F., & McElligott, A. G. (2013) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2013.03.007 · Cited by 64 · see citing works
Kranendonk, G., Hopster, H., Fillerup, M., Ekkel, E. D., Mulder, E. J. H., & Taverne, M. A. M. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.12.008 · Cited by 63 · see citing works
The neuropeptide Drosulfakinin regulates social isolation-induced aggression in Drosophila
Agrawal, P., Kao, D., Chung, P., & Looger, L. L. (2020) · Journal of Experimental Biology · doi:10.1242/jeb.207407 · Cited by 66 · see citing works
Effects of attention and rewarded activity on immune parameters and wound healing in pigs
Ernst, K., Tuchscherer, M., Kanitz, E., Puppe, B., & Manteuffel, G. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.07.001 · Cited by 61 · see citing works
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Ellegaard, L., Cunningham, A., Edwards, S. A., Grand, N., Nevalainen, T. O., Prescott, M. J., & Schuurman, T. (2010) · Journal of Pharmacological and Toxicological Methods · doi:10.1016/j.vascn.2010.05.006 · Cited by 61 · see citing works
A Proposed Role for Pro-Inflammatory Cytokines in Damaging Behavior in Pigs
Nordgreen, J., Edwards, S. A., Boyle, L. A., Bolhuis, J. E., Veit, C., Sayyari, A., Marin, D. E., Dimitrov, I., Janczak, A. M., & Valros, A. (2020) · Frontiers in Veterinary Science · doi:10.3389/fvets.2020.00646 · Cited by 60 · see citing works
Harrison, E. L., & Baune, B. T. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.31 · Cited by 59 · see citing works
Kanitz, E., Otten, W., & Tuchscherer, M. (2005) · Livestock Production Science · doi:10.1016/j.livprodsci.2004.12.002 · Cited by 59 · see citing works
Self-citationReimert, I., Rodenburg, T. B., Ursinus, W., Kemp, B., & Bolhuis, J. E. (2014) · PLoS ONE · doi:10.1371/journal.pone.0108700 · Cited by 58 · see citing works
Behavioural, endocrine and immune responses to repeated social stress in pregnant gilts
Couret, D., Otten, W., Puppe, B., Prunier, A., & Merlot, É. (2008) · animal · doi:10.1017/s1751731108003236 · Cited by 58 · see citing works
Self-citationPastorelli, G., Rossi, R., & Corino, C. (2012) · Czech Journal of Animal Science · doi:10.17221/6006-cjas · Cited by 56 · see citing works
Loria, A. S., Ho, D. H., & Pollock, J. S. (2014) · Acta Physiologica · doi:10.1111/apha.12189 · Cited by 53 · see citing works
Linking the social environment to illness in farm animals
Proudfoot, K. L., Weary, D. M., & von Keyserlingk, M. A. G. (2012) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2012.02.008 · Cited by 52 · see citing works
Siegford, J. M., Rucker, G., & Zanella, A. J. (2007) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2007.03.022 · Cited by 52 · see citing works
Effects of social isolation on growth, stress response, and immunity of zebrafish
Forsatkar, M. N., Safari, O., & Boiti, C. (2017) · acta ethologica · doi:10.1007/s10211-017-0270-7 · Cited by 52 · see citing works
Pié, S., Awati, A., Vida, S., Falluel, I., Williams, B. A., & Oswald, I. P. (2007) · Journal of Animal Science · doi:10.2527/jas.2006-535 · Cited by 50 · see citing works
Heat and social rank impact behavior and physiology of PRRS-virus-infected pigs
Sutherland, M. A., Niekamp, S. R., Johnson, R. W., Alstine, W. G. V., & Salak‐Johnson, J. L. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.08.029 · Cited by 49 · see citing works
O’Connor, E., Parker, M. O., McLeman, M. A., Demmers, T. G. M., Lowe, J. C., Cui, L., Davey, E. L., Owen, R. C., Wathes, C. M., & Abeyesinghe, S. M. (2010) · animal · doi:10.1017/s1751731110001072 · Cited by 48 · see citing works
Radahmadi, M., Shadan, F., Karimian, S. M., Sadr, S. S.-E.-D., & Nasimi, A. (2005) · Pathophysiology · doi:10.1016/j.pathophys.2005.07.001 · Cited by 48 · see citing works
Sullivan, S., Friess, S. H., Ralston, J., Smith, C., PROPERT, K. J., Rapp, P. E., & Margulies, S. S. (2012) · Journal of Neurotrauma · doi:10.1089/neu.2012.2594 · Cited by 48 · see citing works
Changes in endocrine and immune responses of neonatal pigs exposed to a psychosocial stressor
Tuchscherer, M., Kanitz, E., Puppe, B., Tuchscherer, A., & Viergutz, T. (2009) · Research in Veterinary Science · doi:10.1016/j.rvsc.2009.04.010 · Cited by 49 · see citing works
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Düpjan, S., Ramp, C., Kanitz, E., Tuchscherer, A., & Puppe, B. (2013) · Journal of Veterinary Behavior · doi:10.1016/j.jveb.2013.05.007 · Cited by 47 · see citing works
Self-citationKanitz, E., Tuchscherer, M., Otten, W., Tuchscherer, A., Zebunke, M., & Puppe, B. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00173 · Cited by 46 · see citing works
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Düpjan, S., Tuchscherer, A., Langbein, J., Schön, P.-C., Manteuffel, G., & Puppe, B. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.03.017 · Cited by 46 · see citing works
Self-citationTuchscherer, M., Kanitz, E., Puppe, B., & Tuchscherer, A. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.026 · Cited by 45 · see citing works
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Munsterhjelm, C., Valros, A., Heinonen, M., Hälli, O., Siljander-Rasi, H., & Peltoniemi, O. A. T. (2009) · animal · doi:10.1017/s1751731109990814 · Cited by 45 · see citing works
Otten, W., Kanitz, E., Tuchscherer, M., Puppe, B., & Nürnberg, G. (2006) · Livestock Science · doi:10.1016/j.livsci.2006.08.012 · Cited by 44 · see citing works
Self-citationIntravenous catecholamine administration affects mouse intestinal lymphocyte number and apoptosis
Marra, S., Burnett, M., & Hoffman‐Goetz, L. (2004) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2004.08.008 · Cited by 43 · see citing works
Kerschaver, C. V., Turpin, D. L., Michiels, J., & Pluske, J. R. (2023) · Animals · doi:10.3390/ani13101644 · Cited by 41 · see citing works
Swine Inflammation and Necrosis Syndrome (SINS)
Reiner, G., Kuehling, J., Loewenstein, F., Lechner, M., & Becker, S. (2021) · Animals · doi:10.3390/ani11061670 · Cited by 41 · see citing works
Scharf, I., Stoldt, M., Libbrecht, R., Höpfner, A. L., Jongepier, E., Kever, M., & Foitzik, S. (2021) · Molecular Ecology · doi:10.1111/mec.15902 · Cited by 40 · see citing works
Repeated mixing and isolation: Measuring chronic, intermittent stress in Holstein calves
Wilcox, C. S., Schutz, M. M., Rostagno, M. M., Lay, D. C., Jr., & Eicher, S. D. (2013) · Journal of Dairy Science · doi:10.3168/jds.2013-6944 · Cited by 38 · see citing works
Poessel, S. A., Biggins, D. E., Santymire, R. M., Livieri, T. M., Crooks, K. R., & Angeloni, L. M. (2011) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2011.04.018 · Cited by 37 · see citing works
The Effect of Probiotics on Microbiology, Health and Performance of Fattening Rabbits
Kritas, S. K., Petridou, E., Fortomaris, P. D., Tzika, E. D., Arsenos, G. I., & Koptopoulos, G. (2008) · Asian-Australasian Journal of Animal Sciences · doi:10.5713/ajas.2008.70186 · Cited by 36 · see citing works
Age over experience: Consistency of aggression and mounting behaviour in male and female pigs
Clark, C. C. A., & D’Eath, R. B. (2013) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2013.04.014 · Cited by 36 · see citing works
Long‐term cognitive enrichment affects opioid receptor expression in the amygdala of domestic pigs
Kalbe, C., & Puppe, B. (2009) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2009.00536.x · Cited by 36 · see citing works
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Basile, F., Capaccia, C., Zampini, D., Biagetti, T., Diverio, S., & Guelfi, G. (2020) · Animals · doi:10.3390/ani11010047 · Cited by 34 · see citing works
Li, L., Xia, D., Bao, E., Shi, W., Xiao, J.-S., Bao, J.-W., Chen, W.-H., Chen, J., Hartung, J., & Zhao, R. (2007) · Livestock Science · doi:10.1016/j.livsci.2007.03.008 · Cited by 35 · see citing works
Robinson, K. J., Bosch, O. J., Levkowitz, G., Busch, K. E., Jarman, A. P., & Ludwig, M. (2019) · Journal of Neuroendocrinology · doi:10.1111/jne.12807 · Cited by 33 · see citing works
Tallet, C., Rakotomahandry, M., Herlemont, S., & Prunier, A. (2019) · Frontiers in Veterinary Science · doi:10.3389/fvets.2019.00462 · Cited by 34 · see citing works
Lessons from lonely flies: Molecular and neuronal mechanisms underlying social isolation
Yadav, R. S. P., Ansari, F., Bera, N., Kent, C. F., & Agrawal, P. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105504 · Cited by 34 · see citing works
Poletto, R., Siegford, J. M., Steibel, J. P., Coussens, P. M., & Zanella, A. J. (2005) · Brain Research · doi:10.1016/j.brainres.2005.11.012 · Cited by 31 · see citing works
Meijer, E., van Nes, A., Back, W., & van der Staay, F. J. (2015) · The Veterinary Journal · doi:10.1016/j.tvjl.2015.10.016 · Cited by 30 · see citing works
Neurophysiological and behavioral synchronization in group-living and sleeping mice
Sotelo, M. I., Markunas, C., Kudlak, T., Kohtz, C., Vyssotski, A. L., Rothschild, G., & Eban-Rothschild, A. (2023) · Current Biology · doi:10.1016/j.cub.2023.11.065 · Cited by 36 · see citing works
Harrison, E. L., Jaehne, E. J., Jawahar, M. C., Corrigan, F., & Baune, B. T. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.01.036 · Cited by 29 · see citing works
Esquifino, A. I., Cano, P., Jiménez‐Ortega, V., Fernández‐Mateos, P., & Cardinali, D. P. (2007) · Endocrine · doi:10.1007/s12020-007-9009-y · Cited by 29 · see citing works
Sánchez, J., Matas-Quintanilla, M., Ibáñez‐López, F. J., Hernández, I., Sotillo, J., & Gutiérrez, A. M. (2022) · Frontiers in Veterinary Science · doi:10.3389/fvets.2022.881435 · Cited by 29 · see citing works
Tallet, C., Brajon, S., Devillers, N., & Lensink, J. (2017) · Elsevier eBooks · doi:10.1016/b978-0-08-101012-9.00008-3 · Cited by 28 · see citing works
Stress Biomarkers in Pigs: Current Insights and Clinical Application
Papatsiros, V. G., Maragkakis, G., & Papakonstantinou, G. I. (2024) · Veterinary Sciences · doi:10.3390/vetsci11120640 · Cited by 27 · see citing works
Lifetime consequences of the early physical and social environment of piglets
Telkänranta, H., & Edwards, S. A. (2017) · Elsevier eBooks · doi:10.1016/b978-0-08-101012-9.00013-7 · Cited by 27 · see citing works
Kaiser, E. E., Waters, E. S., Fagan, M. M., Scheulin, K. M., Platt, S. R., Jeon, J. H., Fang, X., Kinder, H. A., Shin, S. K., Duberstein, K. J. J., et al. (2020) · Brain Research · doi:10.1016/j.brainres.2020.146778 · Cited by 26 · see citing works
Turpin, D. L., Langendijk, P., Chen, T., & Pluske, J. R. (2016) · Animals · doi:10.3390/ani6110066 · Cited by 26 · see citing works
Weedman, S. M., Rostagno, M. H., Patterson, J. A., Yoon, I., Fitzner, G. E., & Eicher, S. D. (2011) · Journal of Animal Science · doi:10.2527/jas.2009-2539 · Cited by 26 · see citing works
Fil, J. E., Joung, S., Hayes, C. A., & Dilger, R. N. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.649536 · Cited by 25 · see citing works
Indicadores do bem-estar em suínos
Baptista, R. I. A. D. A., Bertani, G. R., & Barbosa, C. N. (2011) · Ciência Rural · doi:10.1590/s0103-84782011005000133 · Cited by 25 · see citing works
Ji, W., Bi, Y., Cheng, Z., Liu, R., Zhang, X., Shu, Y., Li, X., Bao, J., & Liu, H. (2021) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2021.105314 · Cited by 24 · see citing works
Reiske, L., Schmucker, S. S., Pfaffinger, B., Weiler, U., Steuber, J., & Stefanski, V. (2020) · The Journal of Immunology · doi:10.4049/jimmunol.2000269 · Cited by 24 · see citing works
New policies on skin-to-skin contact warrant an oxytocin-based perspective on perinatal health care
Bergman, N. (2024) · Frontiers in Psychology · doi:10.3389/fpsyg.2024.1385320 · Cited by 23 · see citing works
Altered Immunomodulation by Glucocorticoids in Neonatal Pigs Exposed to a Psychosocial Stressor
Tuchscherer, M., Kanitz, E., Puppe, B., & Tuchscherer, A. (2010) · Pediatric Research · doi:10.1203/pdr.0b013e3181f70f08 · Cited by 24 · see citing works
Self-citationMcMillan, F. D. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.09.013 · Cited by 23 · see citing works
Schulz, M., Zieglowski, L., Kopaczka, M., & Tolba, R. H. (2022) · European Surgical Research · doi:10.1159/000525680 · Cited by 22 · see citing works
A novel method for testing social recognition in young pigs and the modulating effects of relocation
Souza, A. S., Jansen, J., Tempelman, R. J., Mendl, M., & Zanella, A. J. (2005) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2005.09.008 · Cited by 22 · see citing works
Influence of teeth resection on the skin temperature and acute phase response in newborn piglets
Moya, S. L., Boyle, L. A., Lynch, P. B., & Arkins, S. (2006) · Animal Welfare · doi:10.1017/s0962728600030499 · Cited by 22 · see citing works
Marchant, J. N., & Herskin, M. S. (2017) · Elsevier eBooks · doi:10.1016/b978-0-08-101012-9.00015-0 · Cited by 21 · see citing works
Early ontogeny social deprivation modifies future agonistic behaviour in crayfish
Patoka, J., Kalous, L., & Bartoš, L. (2019) · Scientific Reports · doi:10.1038/s41598-019-41333-8 · Cited by 21 · see citing works
- Authors
- Kanitz, E., Tuchscherer, M., Puppe, B., Tuchscherer, A., & Stabenow, B.
- Affiliations
- Research Institute for Farm Animal Biology (FBN) (DE)
- Corresponding author
- Kanitz, Ellen
- Venue
- Brain, Behavior, and Immunity
- Publisher
- Elsevier BV
- Published
- 2004-01
- Volume
- 18
- Issue
- 1
- Pages
- 35-45
- ISSN
- 0889-1591 (ISSN-L)
- OpenAlex
- W2008615421
- Cited by
- 200
- References
- 71
- Citations by year
- 2026: 3 · 2025: 9 · 2024: 6 · 2023: 11 · 2022: 8 · 2021: 8 · 2020: 14 · 2019: 9 · 2018: 5 · 2017: 8 · 2016: 12 · 2015: 4 · 2014: 9 · 2013: 17 · 2012: 4
- FWCI
- 11.57
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain Behavior and Immunity (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- Topics
- Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- piglets, maternal deprivation, neuroendocrine stress response, hypothalamic-pituitary-adrenal axis, cortisol, ACTH, glucocorticoid receptor, IL-1β, hippocampus, lymphocyte proliferation, open field behavior, neuroimmune interactions, animal welfare, animal models
- MeSH terms
- Adrenocorticotropic Hormone, Amygdala, Analysis of Variance, Animals, Corticotropin-Releasing Hormone, Exploratory Behavior, Female, Hippocampus, Hydrocortisone, Hypothalamo-Hypophyseal System, Hypothalamus, Immune System, Interleukin-1, Lymphocyte Activation, Male, Maternal Deprivation, Pituitary-Adrenal System, Social Isolation, Stress, Psychological, Neuroimmunomodulation, Sus scrofa
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