Social stress as a cause of diseases in farm animals: Current knowledge and future directions

Veterinary Journal

Volumn 206, Issue 1, 2015, Pages 15-21

  Proudfoot, Kathryn ^a   Habing, Gregory ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Illness; Livestock; Overstocking; Regrouping; Social isolation

Indexed keywords

CATECHOLAMINE; CORTICOTROPIN; GLUCOCORTICOID RECEPTOR; HYDROCORTISONE;

AGGRESSION; ANIMAL DISEASE; ANIMAL SALMONELLOSIS; BACTERIAL GROWTH; BACTERIAL SHEDDING; BACTERIAL VIRULENCE; BOVINE HERPESVIRUS 1; CATECHOLAMINE URINE LEVEL; CHRONIC STRESS; CONFLICT; COPING BEHAVIOR; CROWDING (AREA); EARLY LIFE STRESS; EXPLORATORY BEHAVIOR; FARM ANIMAL; HERPES VIRUS INFECTION; LYMPHOCYTE PROLIFERATION; MORTALITY; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; NONHUMAN; PATHOGENESIS; PNEUMONIC PASTEURELLOSIS; PROTEIN BINDING; PSEUDORABIES; REVIEW; SALIVA LEVEL; SALMONELLA; SOCIAL ISOLATION; SOCIAL STATUS; SOCIAL STRESS; ANIMAL; ANIMAL WELFARE; LIVESTOCK; MENTAL STRESS; PSYCHOLOGY; SOCIAL BEHAVIOR;

ANIMAL DISEASES; ANIMAL WELFARE; ANIMALS; LIVESTOCK; SOCIAL BEHAVIOR; STRESS, PSYCHOLOGICAL;

EID: 84941936563     PISSN: 10900233     EISSN: 15322971     Source Type: Journal    
DOI: 10.1016/j.tvjl.2015.05.024     Document Type: Review

References (82)

1. Aich P., Potter A., Griebel P. Modern approaches to understanding stress and disease susceptibility: A review with special emphasis on respiratory disease. International Journal of General Medicine 2009, 2:19-32.
2. Anisman H., Matheson K. Stress, depression, and anhedonia: Caveats concerning animal models. Neuroscience and Biobehavioral Reviews 2005, 29:525-546.
3. Bailey M.T., Dowd S.E., Galley J.D., Hufnagle A.R., Allen R.G., Lyte M. Exposure to a social stressor alters the structure of the intestinal microbiota: Implications for stressor-induced immunomodulation. Brain, Behavior, and Immunity 2011, 25:397-407.
4. Bartolomucci A. Social stress, immune functions and disease in rodents. Frontiers in Neuroendocrinology 2007, 28:28-49.
5. Bearson B.L., Bearson S.M.D. The role of the QseC quorum-sensing sensor kinase in colonization and norepinephrine-enhanced motility of Salmonella enterica serovar Typhimurium. Microbial Pathogenesis 2008, 44:271-278.
6. Beattie V.E., Walker N., Sneddon I.A. An investigation of the effect of environmental enrichment and space allowance on the behaviour and production of growing pigs. Applied Animal Behaviour Science 1996, 48:151-158.
7. Beery A.K., Kaufer D. Stress, social behavior, and resilience: Insights from rodents. Neurobiology of Stress 2015, 1:116-127.
8. Bøe K.E., Berg S., Andersen I.L. Resting behaviour and displacements in ewes - effects of reduced lying space and pen shape. Applied Animal Behaviour Science 2006, 98:249-259.
9. Callaway T., Morrow J. Social stress increases fecal shedding of Salmonella typhimurium by early weaned piglets. Current Issues in Intestinal Microbiology 2006, 7:65-72.
10. Carbonaro D., Friend T., Dellmeier G., Nuti L. Behavioral and physiological responses of dairy goats to isolation. Physiology and Behavior 1992, 51:297-301.
11. Cohen S., Williamson G.M. Stress and infectious disease in humans. Psychological Bulletin 1991, 109:5-24.
12. Collings L.K.M., Weary D.M., Chapinal N., von Keyserlingk M.A.G. Temporal feed restriction and overstocking increase competition for feed by dairy cattle. Journal of Dairy Science 2011, 94:5480-5486.
13. Coutellier L., Arnould C., Boissy A., Orgeur P., Prunier A., Veissier I., Meunier-Salaün M.-C. Pig's responses to repeated social regrouping and relocation during the growing-finishing period. Applied Animal Behaviour Science 2007, 105:102-114.
14. De Groot J., Ruis M.A., Scholten J.W., Koolhaas J.M., Boersma W.J. Long-term effects of social stress on antiviral immunity in pigs. Physiology and Behavior 2001, 73:145-158.
15. De Jong I.C., Ekkel E.D., van de Burgwal J.A., Lambooij E., Korte S.M., Ruis M.A.W., Koolhaas J.M., Blokhuis H.J. Effects of straw bedding on physiological responses to stressors and behavior in growing pigs. Physiology and Behavior 1998, 64:303-310.
16. De Paula Vieira A., de Passillé A.M., Weary D.M. Effects of the early social environment on behavioral responses of dairy calves to novel events. Journal of Dairy Science 2012, 95:5149-5155.
17. DeVries T.J., von Keyserlingk M.A.G., Weary D.M. Effect of feeding space on the inter-cow distance, aggression, and feeding behavior of free-stall housed lactating dairy cows. Journal of Dairy Science 2004, 87:1432-1438.
18. D'Eath R.B. Socialising piglets before weaning improves social hierarchy formation when pigs are mixed post-weaning. Applied Animal Behaviour Science 2005, 93:199-211.
19. Ewbank R., Bryant M.J. Aggressive behaviour amongst groups of domesticated pigs kept at various stocking rates. Animal Behaviour 1972, 20:21-28.
20. Færevik G., Jensen M.B., Bøe K.E. Dairy calves social preferences and the significance of a companion animal during separation from the group. Applied Animal Behaviour Science 2006, 99:205-221.
21. Fraser D., Kramer D.L., Pajor E.A., Weary D.M. Conflict and cooperation: Sociobiological principles and the behaviour of pigs. Applied Animal Behaviour Science 1995, 44:139-157.
22. Fregonesi J.A., Tucker C.B., Weary D.M. Overstocking reduces lying time in dairy cows. Journal of Dairy Science 2007, 90:3349-3354.
23. Gaillard C., Meagher R.K., von Keyserlingk M.A.G., Weary D.M. Social housing improves dairy calves' performance in two cognitive tests. PLoS ONE 2014, 9:e90205.
24. Haley D. The effects of weaning beef calves in two stages on their behavior and growth rate. Journal of Animal Science 2005, 83:2205-2214.
25. Hall F.S. Social deprivation of neonatal, adolescent, and adult rats has distinct neurochemical and behavioral consequences. Critical Reviews in Neurobiology 1998, 12:129-162.
26. Herskin M.S., Jensen K.H. Effects of different degrees of social isolation on the behaviour of weaned piglets kept for experimental purposes. Animal Welfare 2000, 9:237-249.
27. Hessing M.J.C., Scheepens C.J.M., Schouten W.G.P., Tielen M.J.M., Wiepkema P.R. Social rank and disease susceptibility in pigs. Veterinary Immunology and Immunopathology 1994, 43:373-387.
28. Hodgson P.D., Aich P., Manuja A., Hokamp K., Roche F.M., Brinkman F.S.L., Potter A., Babiuk L.A., Griebel P.J. Effect of stress on viral-bacterial synergy in bovine respiratory disease: Novel mechanisms to regulate inflammation. Comparative and Functional Genomics 2005, 6:244-250.
29. Hodgson P.D., Aich P., Stookey J., Popowych Y., Potter A., Babiuk L., Griebel P.J. Stress significantly increases mortality following a secondary bacterial respiratory infection. Veterinary Research 2012, 43:21.
30. Hopster H., van der Werf J.T.N., Blokhuis H.J. Stress enhanced reduction in peripheral blood lymphocyte numbers in dairy cows during endotoxin-induced mastitis. Veterinary Immunology and Immunopathology 1998, 66:83-97.
31. Huzzey J.M., Grant R.J., Overton T.R. Short communication: Relationship between competitive success during displacements at an overstocked feed bunk and measures of physiology and behavior in Holstein dairy cattle. Journal of Dairy Science 2012, 95:4434-4441.
32. Huzzey J.M., Nydam D.V., Grant R.J., Overton T.R. The effects of overstocking Holstein dairy cattle during the dry period on cortisol secretion and energy metabolism. Journal of Dairy Science 2012, 95:4421-4433.
33. Hyun Y., Ellis M., Curtis S., Johnson R. Environmental temperature, space allowance, and regrouping: Additive effects of multiple concurrent stressors in growing pigs. Journal of Swine Health Production 2005, 13:131-138.
34. Kanitz E., Tuchscherer M., Puppea B., Tuchscherer A., Stabenowa B. Consequences of repeated early isolation in domestic piglets (Sus scrofa) on their behavioural, neuroendocrine, and immunological responses. Brain, Behavior, and Immunity 2004, 18:35-45.
35. Keckeis K., Lepschy M., Schöpper H., Moser L., Troxler J., Palme R. Hair cortisol: A parameter of chronic stress? Insights from a radiometabolism study in guinea pigs. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 2012, 182:985-996.
36. Kondo S., Sekine J., Okubo M., Asahida Y. The effect of group size and space allowance on the agonistic and spacing behavior of cattle. Applied Animal Behaviour Science 1989, 24:127-135.
37. Koolhaas J.M., Korte S.M., De Boer S.F., Van Der Vegt B.J., Van Reenen C.G., Hopster H., De Jong I.C., Ruis M.A., Blokhuis H.J. Coping styles in animals: Current status in behavior and stress-physiology. Neuroscience and Biobehavioral Reviews 1999, 23:925-935.
38. Krawczel P.D., Klaiber L.B., Butzler R.E., Klaiber L.M., Dann H.M., Mooney C.S., Grant R.J. Short-term increases in stocking density affect the lying and social behavior, but not the productivity, of lactating Holstein dairy cows. Journal of Dairy Science 2012, 95:4298-4308.
39. Kroenke C.H., Quesenberry C., Kwan M.L., Sweeney C., Castillo A., Caan B.J. Social networks, social support, and burden in relationships, and mortality after breast cancer diagnosis in the Life After Breast Cancer Epidemiology (LACE) study. Breast Cancer Research and Treatment 2013, 137:261-271.
40. LeBlanc S.J., Lissemore K.D., Kelton D.F., Duffield T.F., Leslie K.E. Major advances in disease prevention in dairy cattle. Journal of Dairy Science 2006, 89:1267-1279.
41. MacKinnon D., Fairchild A., Fritz M. Mediation analysis. Annual Review of Psychology 2007, 58:593.
42. Macrì S., Chiarotti F., Würbel H. Maternal separation and maternal care act independently on the development of HPA responses in male rats. Behavioural Brain Research 2008, 191:227-234.
43. Marchant J.N., Mendl M.T., Rudd A.R., Broom D.M. The effect of agonistic interactions on the heart rate of group-housed sows. Applied Animal Behaviour Science 1995, 46:49-56.
44. McEwen B.S., Gianaros P.J. Central role of the brain in stress and adaptation: Links to socioeconomic status, health, and disease. Annals of the New York Academy of Sciences 2010, 1186:190-222.
45. McGlone J.J., Salak J.L., Lumpkin E.A., Nicholson R.I., Gibson M., Norman R.L. Shipping stress and social status effects on pig performance, plasma cortisol, natural killer cell activity, and leukocyte numbers. Journal of Animal Science 1993, 71:888-896.
46. Mench J., Swanson J., Stricklin W. Social stress and dominance among group members after mixing beef cows. Canadian Journal of Animal Science 1990, 70:345-354.
47. Moennig V., Floegel-Niesmann G., Greiser-Wilke I. Clinical signs and epidemiology of classical swine fever: A review of new knowledge. The Veterinary Journal 2003, 165:11-20.
48. Moinard C., Mendl M., Nicol C., Green L. A case control study of on-farm risk factors for tail biting in pigs. Applied Animal Behaviour Science 2003, 81:333-355.
49. Möstl E., Palme R. Hormones as indicators of stress. Domestic Animal Endocrinology 2002, 23:67-74.
50. Otten W., Puppe B., Kanitz E., Schon P.C., Stabenow B. Effects of dominance and familiarity on behaviour and plasma stress hormones in growing pigs during social confrontation. Journal of Veterinary Medicine 1999, 46:277-292.
51. Pitts A.D., Weary D.M., Pajor E.A., Fraser D. Mixing at young ages reduces fighting in unacquainted domestic pigs. Applied Animal Behaviour Science 2000, 68:191-197.
52. Proudfoot K.L., Veira D.M., Weary D.M., von Keyserlingk M.A.G. Competition at the feed bunk changes the feeding, standing, and social behavior of transition dairy cows. Journal of Dairy Science 2009, 92:3116-3123.
53. Rault J.L. Friends with benefits: social support and its relevance to farm animal welfare. Applied Animal Behavior Science 2012, 136:1-14.
54. Raussi S., Boissy A. Repeated regrouping of pair-housed heifers around puberty affects their behavioural and HPA axis reactivities. Animal Research 2006, 55:131-144.
55. Remience V., Wavreille J., Canart B., Meunier-Salaün M.-C., Prunier A., Bartiaux-Thill N., Nicks B., Vandenheede M. Effects of space allowance on the welfare of dry sows kept in dynamic groups and fed with an electronic sow feeder. Applied Animal Behaviour Science 2008, 112:284-296.
56. Ruis M., Tebrake J., Engel B., Buist W., Blokhuis H., Koolhaas J. Adaptation to social isolation: Acute and long-term stress responses of growing gilts with different coping characteristics. Physiology and Behavior 2001, 73:541-551.
57. Rushen J. Problems associated with the interpretation of physiological data in the assessment of animal welfare. Applied Animal Behaviour Science 1991, 28:381-386.
58. Rushen J., Boissy A., Terlouw E.M., de Passille A.M. Opioid peptides and behavioral and physiological responses of dairy cows to social isolation in unfamiliar surroundings. Journal of Animal Science 1999, 77:2918-2924.
59. Salak-Johnson J.L., McGlone J.J. Making sense of apparently conflicting data: Stress and immunity in swine and cattle. Journal of Animal Science 2007, 85:E81-E88.
60. Sapolsky R.M., Michael Romero L., Munck A.U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews 2000, 21:55-89.
61. Schirmann K., Chapinal N., Weary D.M., Heuwieser W., von Keyserlingk M.A.G. Short-term effects of regrouping on behavior of prepartum dairy cows. Journal of Dairy Science 2011, 94:2312-2319.
62. Schwartz S., Meyer I.H. Mental health disparities research: The impact of within and between group analyses on tests of social stress hypotheses. Social Science and Medicine 2010, 70:1111-1118.
63. Sevi A., Taibi L., Albenzio M., Muscio A., Dell'Aquila S., Napolitano F. Behavioral, adrenal, immune, and productive responses of lactating ewes to regrouping and relocation. Journal of Animal Science 2001, 79:1457-1465.
64. Seyle H. The Stress of Life 1956, McGraw-Hill, New York.
65. Silva P., Moraes J. Effects of weekly regrouping of prepartum dairy cows on innate immune response and antibody concentration. Journal of Dairy Science 2013, 96:7649-7657.
66. Silva P., Dresch A., Machado K. Prepartum stocking density: Effects on metabolic, health, reproductive, and productive responses. Journal of Dairy Science 2014, 97:5521-5532.
67. Spoolder H.A., Edwards S., Corning S. Aggression among finishing pigs following mixing in kennelled and unkennelled accommodation. Livestock Production Science 2000, 63:121-129.
68. Stecher B., Chaffron S., Käppeli R., Hapfelmeier S., Freedrich S., Weber T.C., Kirundi J., Suar M., McCoy K.D., von Mering C., et al. Like will to like: Abundances of closely related species can predict susceptibility to intestinal colonization by pathogenic and commensal bacteria. PLoS Pathogens 2010, 6:e1000711.
69. Stookey J.M., Gonyou H.W. The effects of regrouping on behavioral and production parameters in finishing swine. Journal of Animal Science 1994, 72:2804-2811.
70. Stringhini S., Dugravot A., Shipley M., Goldberg M., Zins M., Kivimäki M., Marmot M., Sabia S., Singh-Manoux A. Health behaviours, socioeconomic status, and mortality: Further analyses of the British Whitehall II and the French GAZEL prospective cohorts. PLoS Medicine 2011, 8:e1000419.
71. Sutherland M.A., Niekamp S.R., Rodriguez-Zas S.L., Salak-Johnson J.L. Impacts of chronic stress and social status on various physiological and performance measures in pigs of different breeds. Journal of Animal Science 2006, 84:588-596.
72. Talebi A., von Keyserlingk M.A.G., Telezhenko E., Weary D.M. Reduced stocking density mitigates the negative effects of regrouping in dairy cattle. Journal of Dairy Science 2014, 97:1358-1363.
73. Tempelman R.J. Invited review: Assessing experimental designs for research conducted on commercial dairies. Journal of Dairy Science 2009, 92:1-15.
74. Tennessen T., Price M.A., Berg R.T. The social interactions of young bulls and steers after re-grouping. Applied Animal Behaviour Science 1985, 14:37-47.
75. Toscano M.J., Stabel T.J., Bearson S.M.D., Bearson B.L., Lay D.C. Cultivation of Salmonella enterica serovar Typhimurium in a norepinephrine-containing medium alters in vivo tissue prevalence in swine. Journal of Experimental Animal Science 2007, 43:329-338.
76. Tuchscherer M., Kanitz E., Puppe B., Tuchscherer A., Viergutz T. Changes in endocrine and immune responses of neonatal pigs exposed to a psychosocial stressor. Research in Veterinary Science 2009, 87:380-388.
77. Turner S.P., Ewen M., Rooke J.A., Edwards S.A. The effect of space allowance on performance, aggression and immune competence of growing pigs housed on straw deep-litter at different group sizes. Livestock Production Science 2000, 66:47-55.
78. Uchino B.N. Social support and health: A review of physiological processes potentially underlying links to disease outcomes. Journal of Behavioral Medicine 2006, 29:377-387.
79. von Keyserlingk M.A.G., Olenick D., Weary D.M. Acute behavioral effects of regrouping dairy cows. Journal of Dairy Science 2008, 91:1011-1016.
80. Vandenheede M., Bouissou M.F., Picard M. Interpretation of behavioural reactions of sheep towards fear-eliciting situations. Applied Animal Behaviour Science 1998, 58:293-310.
81. Weary D., Fraser D. Social and reproductive behavior. The Ethology of Domestic Animals: An Introductory Text 2009, 73-83. CABI, Cambridge. P. Jensen (Ed.).
82. Wilcox C.S., Schutz M.M., Rostagno M.R., Lay D.C., Eicher S.D. Repeated mixing and isolation: Measuring chronic, intermittent stress in Holstein calves. Journal of Dairy Science 2013, 96:7223-7233.