Different stressors elicit different responses in the salivary biomarkers cortisol, haptoglobin, and chromogranin A in pigs

Research in Veterinary Science

Volumn 97, Issue 1, 2014, Pages 124-128

  Ott, S ^a,b   Soler, L ^a   Moons, C P H ^b   Kashiha, M A ^a   Bahr, C ^a   Vandermeulen, J ^a   Janssens, S ^a   Gutierrez A M ^c   Escribano, D ^c   Ceron J J ^c   Berckmans, D ^a   Tuyttens, F A M ^b,d   Niewold, T A ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c UNIVERSITY OF MURCIA   (Spain)

^d INSTITUTE FOR AGRICULTURAL AND FISHERIES RESEARCH ILVO   (Belgium)

Author keywords

Chromogranin A; Cortisol; Haptoglobin; Pig; Saliva; Stress

Indexed keywords

BIOLOGICAL MARKER; CHROMOGRANIN A; HAPTOGLOBIN; HYDROCORTISONE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CORRELATIONAL STUDY; FOOD DEPRIVATION; NONHUMAN; PHYSIOLOGICAL STRESS; SALIVA ANALYSIS; SALIVA LEVEL; SKIN DEFECT; SWINE; WEIGHT GAIN; ANIMAL; CONTROLLED CLINICAL TRIAL; CROWDING (AREA); FLUOROIMMUNOASSAY; IMMUNOASSAY; METABOLISM; PHYSIOLOGY; PIG; SALIVA; STATISTICAL MODEL; VETERINARY;

SUIDAE;

ANIMALS; BIOLOGICAL MARKERS; CHROMOGRANIN A; CROWDING; FLUOROIMMUNOASSAY; FOOD DEPRIVATION; HAPTOGLOBINS; HYDROCORTISONE; IMMUNOASSAY; LINEAR MODELS; SALIVA; STRESS, PHYSIOLOGICAL; SUS SCROFA; SWINE;

EID: 84905241871     PISSN: 00345288     EISSN: 15322661     Source Type: Journal    
DOI: 10.1016/j.rvsc.2014.06.002     Document Type: Article

References (43)

1. Aninat C., Seguin P., Descheemaeker P.N., Morel F., Malledant Y., Guillouzo A. Catecholamines induce an inflammatory response in human hepatocytes. Critical Care Medicine 2008, 36:848-854.
2. Black P.H. Stress and the inflammatory response: a review of neurogenic inflammation. Brain, Behavior, and Immunity 2002, 16:622-653.
3. Bürger W., Ewald C., Fennert E.M. Increase in C-reactive protein in the serum of piglets (pCRP) following ACTH or corticosteroid administration. Journal of Veterinary Medicine, Series B 1998, 45:1-6.
4. Coutellier L., Arnould C., Boissy A., Orgeur P., Prunier A., Veissier I., et al. Pig's responses to repeated social regrouping and relocation during the growing-finishing period. Applied Animal Behaviour Science 2007, 105:102-114.
5. de Groot J., Ruis M.A.W., Scholten J.W., Koolhaas J.M., Boersma W.J.A. Long-term effects of social stress on antiviral immunity in pigs. Physiology & Behavior 2001, 73:145-158.
6. Escribano D., Fuentes-Rubio M., Cerón J.J. Validation of an automated chemiluminescent immunoassay for salivary cortisol measurements in pigs. Journal of Veterinary Diagnostic Investigation 2012, 24:918-923.
7. Escribano D., Soler L., Gutiérrez A.M., Martinez-Subiela S., Cerón J.J. Measurement of chromogranin A in porcine saliva: validation of a time-resolved immunofluorometric assay and evaluation of its application as a marker of acute stress. Animal 2013, 7:640-647.
8. Escribano D., Gutiérrez A.M., Fuentes-Rubio M., Cerón J.J. Saliva chromogranin A in growing pigs: a study of circadian patterns during daytime and stability under different storage conditions. The Veterinary Journal 2014, in press.
9. Fernandez X., Meunier-Salaün M.C., Ecolan P., Mormède P. Interactive effect of food deprivation and agonistic behavior on blood parameters and muscle glycogen in pigs. Physiology & Behavior 1995, 58:337-345.
10. Ferraris R.P., Carey H.V. Intestinal transport during fasting and malnutrition. Annual Reviews Nutrition 2000, 20:195-219.
11. Gallina S., Di Mauro M., D'Amico M.A., D'Angelo E., Sablone A., Di Fonso A., et al. Salivary chromogranin A, but not alfa-amylase, correlates with cardiovascular parameters during high-intensity exercise. Clinical Endocrinology 2011, 75:747-752.
12. Gómez-Laguna J., Gutiérrez A.M., Pallarés F.J., Salguero F.J., Cerón J.J., Carrasco L. Haptoglobin and C-reactive protein as biomarkers in the serum, saliva and meat juice of pigs experimentally infected with porcine reproductive and respiratory syndrome virus. The Veterinary Journal 2010, 185:83-87.
13. Gruys E., Toussain M.J.M., Niewold T.A., Koopmans S.J. Acute phase reaction and acute phase proteins. Journal of Zhejiang University. Science 2005, 6B:1045-1056.
14. Gutiérrez A.M., Martínez-Subiela S., Cerón J.J. Evaluation of an immunoassay for determination of haptoglobin concentration in various biological specimens from swine. American Journal of Veterinary Research 2009, 70:691-696.
15. Gutiérrez A.M., Escribano D., Fuentes M., Cerón J.J. Circadian pattern of acute phase proteins in the saliva of growing pigs. The Veterinary Journal 2013, 196:167-170.
16. Hyun Y., Ellis M., Riskowski G., Johnson R.W. Growth performance of pigs subjected to multiple concurrent environmental stressors. Journal of Animal Science 1998, 76:721-727.
17. Kanno T., Asada N., Yanase H., Iwanaga T., Ozaki T., Nishikawa Y., et al. Salivary secretion of highly concentrated chromogranin a in response to noradrenaline and acetylcholine in isolated and perfused rat submandibular glands. Experimental Physiology 1999, 84:1073-1083.
18. Kirschbaum C., Hellhammer D.H. Salivary cortisol in psychoneuroendocrine research: recent developments and applications. Psychoneuroendocrinology 1994, 19:313-333.
19. Koolhaas J.M., Bartolomucci A., Buwalda B., de Boer S.F., Flügge G., Korte S.M., et al. Stress revisited: a critical evaluation of the stress concept. Neuroscience & Biobehavioral Reviews 2011, 35:1291-1301.
20. Lallès J.P., David J.C. Fasting and refeeding modulate the expression of stress proteins along the gastrointestinal tract of weaned pigs. Journal of Animal Physiology and Animal Nutrition 2011, 95:478-488.
21. Lee T., Shimizu T., Iijima M., Obinata K., Yamashiro Y., Nagasawa S. Evaluation of psychosomatic stress in children by measuring salivary chromogranin A. Acta Pædiatrica 2006, 95:935-939.
22. Merlot E., Meunier-Salaün M.C., Prunier A. Behavioural, endocrine and immune consequences of mixing in weaned piglets. Applied Animal Behaviour Science 2004, 85:247-257.
23. Merlot E., Mounier A.M., Prunier A. Endocrine response of gilts to various common stressors: a comparison of indicators and methods of analysis. Physiology & Behavior 2011, 102:259-265.
24. Mormède P., Andanson S., Aupérin B., Beerda B., Guémené D., Malmkvist J., et al. Exploration of the hypothalamic-pituitary-adrenal function as a tool to evaluate animal welfare. Physiology & Behavior 2007, 92:317-339.
25. Murata H., Shimada N., Yoshioka M. Current research on acute phase proteins in veterinary diagnosis: an overview. The Veterinary Journal 2004, 168:28-40.
26. Nakane H., Asami O., Yamada Y., Harada T., Matsui N., Kanno T., et al. Salivary chromogranin A as an index of psychosomatic stress. Biomedical Research 1998, 19:401-406.
27. Obayashi K. Salivary mental stress proteins. Clinica Chimica Acta 2013, 425:196-201.
28. Piñeiro C., Morales J., Piñeiro M., Lampreave F., Mateos G.G. Effects of induced mixing and pen size on performance and serum concentration of acute phase proteins in growing pigs. Journal of Animal Science 2004, 82:505.
29. Piñeiro C., Piñeiro M., Morales J., Carpintero R., Campbell F.M., Eckersall P.D., et al. Pig acute-phase protein levels after stress induced by changes in the pattern of food administration. Animal 2007, 1:133-139.
30. Piñeiro M., Piñeiro C., Carpintero R., Morales J., Campbell F.M., Eckersall P.D., et al. Characterisation of the pig acute phase protein response to road transport. The Veterinary Journal 2007, 173:669-674.
31. Prunier A., Mounier A.M., Hay M. Effects of castration, tooth resection, or tail docking on plasma metabolites and stress hormones in young pigs. Journal of Animal Science 2005, 83:216-222.
32. Ruis M.A.W., te Brake J.H.A., Engel B., Ekkel E.D., Buist W.G., Blokhuis H.J., et al. The circadian rhythm of salivary cortisol in growing pigs: effects of age, gender, and stress. Physiology & Behavior 1997, 62:623-630.
33. Ruis M.A.W., de Groot J., te Brake J.H.A., Dinand Ekkel E., van de Burgwal J.A., Erkens J.H.F., et al. Behavioural and physiological consequences of acute social defeat in growing gilts: effects of the social environment. Applied Animal Behaviour Science 2001, 70:201-225.
34. Saco Y., Docampo M.J., Fàbrega E., Manteca X., Diestre A., Lampreave F., et al. Effect of transport stress on serum haptoglobin and pig-MAP in pigs. Animal Welfare 2003, 12:403-409.
35. Salamano G., Mellia E., Candiani D., Ingravalle F., Bruno R., Ru G., et al. Changes in haptoglobin, C-reactive protein and pig-MAP during a housing period following long distance transport in swine. The Veterinary Journal 2008, 177:110-115.
36. Saruta J., Tsukinoki K., Sasaguri K., Ishii H., Yasuda M., Osamura Y.R., et al. Expression and localization of chromogranin A gene and protein in human submandibular gland. Cells, Tissues, Organs 2005, 180:237-244.
37. Soler L., Gutiérrez A.M., Escribano D., Fuentes M., Cerón J.J. Response of salivary haptoglobin and serum amyloid A to social isolation and short road transport stress in pigs. Research in Veterinary Science 2013, 95:298-302.
38. Spoolder H.A.M., Edwards S.A., Corning S. Aggression among finishing pigs following mixing in kennelled and unkennelled accommodation. Livestock Production Science 2000, 63:121-129.
39. Toda M., Den R., Nagasawa S., Kitamura K., Morimoto K. Relationship between lifestyle scores and salivary stress markers cortisol and chromogranin A. Archives of Environmental & Occupational Health 2005, 60:266-269.
40. Toscano M.J., Lay D.C., Craig B.A., Pajor E.A. Assessing the adaptation of swine to fifty-seven hours of feed deprivation in terms of behavioral and physiological responses. Journal of Animal Science 2007, 85:441-451.
41. Turner S.P., Farnworth M.J., White I.M.S., Brotherstone S., Mendl M., Knap P., et al. The accumulation of skin lesions and their use as a predictor of individual aggressiveness in pigs. Applied Animal Behaviour Science 2006, 96:245-259.
42. von Borell E. Neuroendocrine integration of stress and significance of stress for the performance of farm animals. Applied Animal Behaviour Science 1995, 44:219-227.
43. Winkler H., Fischer-Colbrie R. The chromogranins A and B: the first 25 years and future perspectives. Neuroscience 1992, 49:497-528.