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The effect of allostatic load on hypothalamic–pituitary–interrenal (HPI) axis before and after secondary vaccination in Atlantic salmon postsmolts (Salmo salar L.)

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Abstract

The experiment consisted of three experimental groups: (1) “vaccine and stress”, (2) “stress and vaccine” and (3) control. All groups have previously been vaccinated 6 months prior to the start of the experiment. At the start of the experiment, the “vaccine and stress” group was vaccinated with Pentium Forte Plus for the second time (25.02.2008) and then given a daily stressor (confinement stressor 267 kg m-3 in 15 min) for a period of 4 weeks. The “stress and vaccine” group was given a similar daily stressor for 4 weeks and then vaccinated for the second time. The control group was neither stressed nor vaccinated a second time. The results indicates that fish in the “stress and vaccine” group may have entered an allostatic overload type 2 due to oversensitivity to ACTH, a reduced efficient negative feedback system with elevated baseline levels of plasma cortisol and reduced immune response with pronounced effects on the well-being of the animal. The “vaccine and stress” group may likewise have entered an allostatic overload type 1 response, with oversensitivity to ACTH and transient reduced efficient negative feedback system. This study shows that if plasma cortisol becomes elevated prior to vaccination, it could perhaps instigate an allostatic overload type 2 with dire consequences on animal welfare. To reduce the risk of compromising the animal welfare during commercial vaccination of salmon, one propose to grade the fish minimum a week prior to vaccination or grade simultaneously with vaccination. This could reduce the overall allostatic load during handling and vaccination and secure a healthy fish with intact immune response and improved animal welfare.

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References

  • Acerete L, Balasch JC, Castellana B, Redruello B, Roher N, Canario AV (2007) Cloning of the glucocorticoid receptor (GR) in gilthead seabream (Sparus aurata). Differential expression of GR and immune genes in gilthead seabream after an immune challenge. Comp Biochem Physiol 148B(1):32–43

    Article  CAS  Google Scholar 

  • Adams A, Thompson KD, Morris D, Farias C, Chen SC (1995) Development and use of monoclonal antibody probes for immunohistochemistry, ELISA and IFAT to detect bacterial and parasitic fish pathogens. Fish Shellfish Immunol 5:537–547

    Article  Google Scholar 

  • Banki CM, Arato M, Papp Z, Rihmer Z, Kovacs Z (1986) Associations among dexamethasone non-suppression and TRH-induced hormonal responses: increased specificity for melancholia. Psychoneuroendocrinology 11(2):205–211

    Article  CAS  PubMed  Google Scholar 

  • Barcellos LJG, Nicolaiewsky S, de Souza SMG, Lulhier F (1999) Plasmatic levels of cortisol in the response to acute stress in Nile tilapia, Oreochromis niloticus (L.), previously exposed to chronic stress. Aquac Res 30(6):437–444

    Article  Google Scholar 

  • Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42(3):517–525

    Article  CAS  PubMed  Google Scholar 

  • Calcagni E, Elenkov I (2006) Stress system activity, innate and T helper cytokines, and susceptibility to immune-related diseases. Ann. N. Y. Acad. Sci.:106962–106976

  • Carmichael GJ (1984) Long distance truck transport of intensively reared largemouth bass. Prog Fish-Cult 46:111–115

    Article  Google Scholar 

  • Castillo J, Castellana B, Acerete L, Planas JV, Goetz FW, Mackenzie S (2008) Stress-induced regulation of steroidogenic acute regulatory protein expression in head kidney of Gilthead seabream (Sparus aurata). J Endocrinol 196(2):313–322

    Article  CAS  PubMed  Google Scholar 

  • Da Rocha RM, Carvalho EG, Urbinati EC (2004) Physiological responses associated with capture and crowding stress in matrinxa Brycon cephalus (Gunther 1869). Aquac Res 35(3):245–249

    Article  Google Scholar 

  • Davis KB, Griffin BR, Gray WL (2002) Effect of handling stress on susceptibility of channel catfish Ictalurus punctatus to Icthyophthirius multifiliis and channel catfish virus infection. Aquaculture 214(1–4):55–66

    Article  Google Scholar 

  • Davis KB, Griffin BR, Gray WL (2003) Effect of dietary cortisol on resistance of channel catfish to infection by Ichthyopthirius multifiliis and channel catfish virus disease. Aquaculture 218(1–4):121–130

    Article  CAS  Google Scholar 

  • Drangsholt TMK, Gjerde B, Ødegård J, Fridell F, Bentsen HB (2011) Quantitative genetics of vaccine-induced side effects in farmed Atlantic salmon (Salmo salar). Aquaculture 318(3–4):316–324

    Article  CAS  Google Scholar 

  • Einarsdottir IE, Nilssen KJ, Iversen M (2000a) Effects of rearing stress on Atlantic salmon (Salmo salar L.) antibody response to a non-pathogenic antigen. Aquac Res 31(12):923–930

    Article  Google Scholar 

  • Einarsdottir IE, Nilssen KJ, Oren SO, Iversen M (2000b) Temperature influence on Arctic charr (Salvelinus alpinus L.) antibody response to a cellular antigen. Polar Biol 23(4):231–235

    Article  Google Scholar 

  • Engelsma MY, Huising MO, van Muiswinkel WB, Flik G, Kwang J, Savelkoul HFJ, Verburg-van Kemenade BML (2002) Neuroendocrine-immune interactions in fish: a role for interleukin-1. Vet Immunol Immunopathol 87(3–4):467–479

    Article  CAS  PubMed  Google Scholar 

  • Engelsma MY, Hougee S, Nap D, Hofenk M, Rombout J, van Muiswinkel WB, Verburg-van Kemenade BML (2003) Multiple acute temperature stress affects leucocyte populations and antibody responses in common carp Cyprinus carpio L. Fish Shellfish Immunol 15(5):397–410

    Article  CAS  PubMed  Google Scholar 

  • Espelid S, Løkken GB, Steiro K, Bøgwald J (1996) Effects of cortisol and stress on the immune system in Atlantic salmon (Salmo salar L.). Fish Shellfish Immunol 6:95–110

    Article  Google Scholar 

  • Fanouraki E, Divanach P, Pavlidis M (2007) Baseline values for acute and chronic stress indicators in sexually immature red porgy (Pagrus pagrus). Aquaculture 265(1–4):294–304

    Article  CAS  Google Scholar 

  • Fast MD, Hosoya S, Johnson SC, Afonso LOB (2008) Cortisol response and immune-related effects of Atlantic salmon (Salmo salar Linnaeus) subjected to short- and long-term stress. Fish Shellfish Immunol 24(2):194–204. doi:10.1016/j.fsi.2007.10.009

    Article  CAS  PubMed  Google Scholar 

  • Fevolden SE, Roed KH, Fjalestad KT (2002) Selection response of cortisol and lysozyme in rainbow trout and correlation to growth. Aquaculture 205(1–2):61–75

    Article  CAS  Google Scholar 

  • Finstad B, Iversen M, Sandodden R (2003) Stress-reducing methods for releases of Atlantic salmon (Salmo salar) smolts in Norway. Aquaculture 222(1–4):203–214

    Article  Google Scholar 

  • Friend TH, Dellmeier GR, Gbur EE (1985) Comparison of four methods of calf confinement. I. Physiology. J Anim Sci 60:1095–1101

    CAS  PubMed  Google Scholar 

  • Funk VA, Jones SRM, Kim E, Kreiberg H, Taylor K, Wu S, Young C (2004) The effect of vaccination and sea water entry on immunocompetence and susceptibility to Kudoa thyrsites in Atlantic salmon (Salmo salar L.). Fish Shellfish Immunol 17(4):375–387

    Article  CAS  PubMed  Google Scholar 

  • Goymann W, Wingfield JC (2004) Allostatic load, social status and stress hormones: the costs of social status matter. Anim Behav 67:591–602. doi:10.1016/j.anbehav.2003.08.007

    Article  Google Scholar 

  • Gudding R, Lillehaug A, Evensen O (1999) Recent developments in fish vaccinology. Vet Immunol Immunopathol 72(1–2):203–212

    Article  CAS  PubMed  Google Scholar 

  • Hasan M, Bart AN (2007) Improved survival of rohu, Labeo rohita (Hamilton-Buchanan) and silver carp, Hypophthalmichthys molitrix (Valenciennes) fingerlings using low-dose quinaldine and benzocaine during transport. Aquac Res 38(1):50–58

    Article  CAS  Google Scholar 

  • Haukenes AH, Barton BA (2004) Characterization of the cortisol response following an acute challenge with lipopolysaccharide in yellow perch and the influence of rearing density. J Fish Biol 64(4):851–862

    Article  CAS  Google Scholar 

  • Holland JW, Pottinger TG, Secombes CJ (2002) Recombinant interleukin-1 beta activates the hypothalamic-pituitary-interrenal axis in rainbow trout Oncorhynchus mykiss. J Endocrin 175(1):261–267

    Article  CAS  Google Scholar 

  • Hoyle I, Oidtmann B, Ellis T, Turnbull J, North B, Nikolaidis J, Knowles TG (2007) A validated macroscopic key to assess fin damage in farmed rainbow trout (Onchorynchus mykiss). Aquac Int 270:142–148

    Article  Google Scholar 

  • Ingram GA (1985) The immune response of brown trout, Salmo trutta to sheep and ‘O’ human erythrocytes. In: Manning MJ, Tatner MF (eds) Fish Immunology Academic Press, London, pp 157–170

  • Iversen M, Finstad B, Nilssen KJ (1998) Recovery from loading and transport stress in Atlantic salmon (Salmo salar L.) smolts. Aquaculture 168(1–4):387–394

    Article  CAS  Google Scholar 

  • Iversen M, Finstad B, McKinley RS, Eliassen RA (2003) The efficacy of metomidate, clove oil, Aqui-S (TM) and Benzoak (R) as anaesthetics in Atlantic salmon (Salmo salar L.) smolts, and their potential stress-reducing capacity. Aquaculture 221(1–4):549–566

    Article  CAS  Google Scholar 

  • Iversen M, Finstad B, McKinley RS, Eliassen RA, Carlsen KT, Evjen T (2005) Stress responses in Atlantic salmon (Salmo salar L.) smolts during commercial well boat transports, and effects on survival after transfer to sea. Aquaculture 243(1–4):373–382

    Article  Google Scholar 

  • Iversen M, Eliassen RA, Finstad B (2009) Potential benefit of clove oil sedation on animal welfare during salmon smolt, Salmo salar L. transport and transfer to sea. Aquac Res 40(2):233–241

    Article  Google Scholar 

  • Janssens CJJG, Helmond FA, Wiegant VM (1994) Increased cortisol response to exogenous adrenocorticotropic hormone in chronically stressed pigs: influence of housing conditions. J Anim Sci 72:1771–1777

    CAS  PubMed  Google Scholar 

  • Juster RP, McEwen BS, Lupien SJ (2010) Allostatic load biomarkers of chronic stress and impact on health and cognition. Neurosci Biobehav Rev 35(1):2–16. doi:10.1016/j.neubiorev.2009.10.002

    Article  PubMed  Google Scholar 

  • Kristoffersen AB, Viljugrein H, Kongtorp RT, Brun E, Jansen PA (2009) Risk factors for pancreas disease (PD) outbreaks in farmed Atlantic salmon and rainbow trout in Norway during 2003-2007. Prev Vet Med 90:127–136

    Article  CAS  PubMed  Google Scholar 

  • Kumar A, Alcser K, Grunhaus L, Greden JF (1986) Relationships of the dexamethasone suppression test to clinical severity and degree of melancholia. Biol Psychiatry 21(5–6):436–444

    Article  CAS  PubMed  Google Scholar 

  • Leatherland JF, Cho CY (1985) Effects of rearing density on thyroid and interregnal gland activity and plasma and hepatic metabolite levels in rainbow trout Salmo gairdneri Richardson. J Fish Biol 27:583–592

    Article  CAS  Google Scholar 

  • Liebert AM, Schreck CB (2006) Effects of acute stress on osmoregulation, feed intake, IGF-1, and cortisol in yearling steelhead trout (Oncorhynchus mykiss) during seawater adaptation. Gen Comp Endocrinol 148(2):195–202

    Article  CAS  PubMed  Google Scholar 

  • Lovy J, Speare DJ, Stryhn H, Wright GM (2008) Effects of dexamethasone on host innate and adaptive immune responses and parasite development in rainbow trout Oncorhynchus mykiss infected with Loma salmonae. Fish Shellfish Immunol 24(5):649–658. doi:10.1016/j.fsi.2008.02.007

    Article  CAS  PubMed  Google Scholar 

  • Maule AG, Schreck CB, Kaattari SL (1987) Changes in the immune system of coho salmon (Oncorhynchus kisutch) during the parr-to-smolt transformation and after implantation of cortisol. Can J Fish Aquat Sci 44:161–166

    Article  CAS  Google Scholar 

  • McEwen BS (1998) Stress, adaptation, and disease - Allostasis and allostatic load. In: Neuroimmunomodulation, vol 840. Ann. N. Y. Acad. Sci.. pp 33-44

  • McEwen BS (2005) Stressed or stressed out: what is the difference? J Psychiatry Neurosci 30(5):315–318

    PubMed Central  PubMed  Google Scholar 

  • McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Horm Behav 43(1):2–15. doi:10.1016/s0018-506x(02)00024-7

    Article  PubMed  Google Scholar 

  • Meunier-Salaun MC, Vantrimponte MN, Raab A, Dantzer R (1987) Effect of floor area restriction upon performance, behavior and physiology of growing finishing pigs. J Anim Sci 64:1371–1377

    CAS  PubMed  Google Scholar 

  • Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9(3):211–268

    Article  Google Scholar 

  • Morgan MJ, Wilson CE, Crim LW (1999) The effect of stress on reproduction in Atlantic cod. J Fish Biol 54(3):477–488

    Article  Google Scholar 

  • Mormede P, Andanson S, Auperin B, Beerda B, Guemene D, Malnikvist J, Manteca X, Manteuffel G, Prunet P, van Reenen CG, Richard S, Veissier I (2007) Exploration of the hypothalamic-pituitary-adrenal function as a tool to evaluate animal welfare. Physiol Behav 92(3):317–339

    Article  CAS  PubMed  Google Scholar 

  • Olsen YA, Einarsdottir IE, Nilssen KJ (1995) Metomidate anaesthesia in Atlantic salmon, Salmo salar, prevents plasma cortisol increase during stress. Aquaculture 134:155–168

    Article  CAS  Google Scholar 

  • Pérez-Casanova JC, Hamoutene D, Samuelson S, Burt K, King TL, Lee K (2010) The immune response of juvenile Atlantic cod (Gadus morhua L.) to chronic exposure to produced water. Mar Environ Res 70(1):26–34

    Article  PubMed  Google Scholar 

  • Pickering AD, Pottinger TG (1989) Stress responses and disease resistance in salmonid fish: effects of chronic elevation of plasma cortisol. Fish Physiol Biochem 7:253–258

    Article  CAS  PubMed  Google Scholar 

  • Portz DE, Woodley CM, Cech JJ (2006) Stress-associated impacts of short-term holding on fishes. Rev Fish Biol Fish 16(2):125–170

    Article  Google Scholar 

  • Pottinger TG, Carrick TR (1999) Modification of the plasma cortisol response to stress in rainbow trout by selective breeding. Gen Comp Endocrinol 116(1):122–132. doi:10.1006/gcen.1999.7355

    Article  CAS  PubMed  Google Scholar 

  • Pottinger TG, Carrick TR (2001) ACTH does not mediate divergent stress responsiveness in rainbow trout. Comp Biochem Physiol 129A(2–3):399–404

    Article  CAS  Google Scholar 

  • Redding MJ, Schreck CB (1983) Influence of ambient salinity on osmoregulation and cortisol concentration in yearling coho salmon during stress. Trans Am Fish Soc 112(6):800–807

    Article  CAS  Google Scholar 

  • Ruane NM, Carballo EC, Komen J (2002) Increased stocking density influences the acute physiological stress response of common carp Cyprinus carpio (L). Aquaculture 210:245–257

    Article  CAS  Google Scholar 

  • Sandodden R, Finstad B, Iversen M (2001) Transport stress in Atlantic salmon (Salmo salar L.): anaesthesia and recovery. Aquac Res 32(2):87–90

    Article  CAS  Google Scholar 

  • Schreck CB (2010) Stress and fish reproduction: the roles of allostasis and hormesis. Gen Comp Endoc 165(3):549–556

    Article  CAS  Google Scholar 

  • Schreck CB, Contreras-Sanchez W, Fitzpatrick MS (2001) Effects of stress on fish reproduction, gamete quality, and progeny. Aquaculture 197(1–4):3–24

    Article  Google Scholar 

  • Selye H (1950) Stress and the general adaption syndrome. Brit Med J 1(4667):1383–1392

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Selye H (1973) Homeostasis and heterostasis. Per Biol Med 16:441–445

    CAS  Google Scholar 

  • Skinner LA, LaPatra SE, Adams A, Thompson KD, Balfry SK, McKinley RS, Schulte PM (2010) Supra-physiological levels of cortisol suppress lysozyme but not the antibody response in Atlantic salmon, Salmo salar L., following vaccine injection. Aquaculture 300(1–4):223–230

    Article  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1987) Introduction to biostatistics. In. Freeman, New York, pp 178–179

    Google Scholar 

  • Stolte EH, Nabuurs SB, Bury NR, Sturm A, Flik G, Savelkoul HFJ, Lidy Verburg-van Kemenade BM (2008) Stress and innate immunity in carp: corticosteroid receptors and pro-inflammatory cytokines. Mol Immunol 46(1):70–79

    Article  CAS  PubMed  Google Scholar 

  • Tanck MWT, Vermeulen KJ, Bovenhuis H, Komen H (2001) Heredity of stress-related cortisol response in androgenetic common carp (Cyprinus carpio L.). Aquaculture 199(3–4):283–294

    Article  CAS  Google Scholar 

  • Tanck MWT, Claes T, Bovenhuis H, Komen J (2002) Exploring the genetic background of stress using isogenic progenies of common carp selected for high or low stress-related cortisol response. Aquaculture 204(3–4):419–434. doi:10.1016/s0044-8486(01)00828-6

    Article  Google Scholar 

  • Tort L (2011) Stress and immune modulation in fish. Dev Comp Immun 35(12):1366–1375

    Article  CAS  Google Scholar 

  • Van Zwol JA, Neff BD, Wilson CC (2012) The influence of non-native salmonids on circulating hormone concentrations in juvenile Atlantic salmon. Anim Behav 83(1):119–129

    Article  Google Scholar 

  • Varsamos S, Flik G, Pepin JF, Bonga SEW, Breuil G (2006) Husbandry stress during early life stages affects the stress response and health status of juvenile sea bass Dicentrarchus labrax. Fish Shellfish Immunol 20(1):83–96

    Article  CAS  PubMed  Google Scholar 

  • Veissier I, Boissy A, De Passille AM, Rushen J, Van Reenen CG, Roussel S (2001) Calves’ responses to repeated social regrouping and relocation. J Anim Sci 79:2580–2593

    CAS  PubMed  Google Scholar 

  • Ventura A, Kusakabe M, Takei Y (2011) Salinity-dependent in vitro effects of homologous natriuretic peptides on the pituitary-interrenal axis in eels. Gen Comp Endoc 173(1):129–138

    Article  CAS  Google Scholar 

  • Vijayan MM, Leatherland JF (1990) High stocking density affects cortisol secretion and tissue distribution in brook charr Salvelinus fontinalis. J endoc 124:311–318

    Article  CAS  Google Scholar 

  • Wendelaar Bonga SE (2011) Hormonal responses to stress. In: Anthony PF (ed) Encyclopedia of fish physiology. Academic Press, San Diego, pp 1515–1523

    Chapter  Google Scholar 

  • Wendelaar Bonga SEW (1997) The stress response in fish. Physiol Rev 77(3):591–625

    Google Scholar 

  • Weyts FAA, Cohen N, Flik G, Verburg-van Kemenade BML (1999) Interactions between the immune system and the hypothalamo-pituitary-interrenal axis in fish. Fish Shellfish Immunol 9(1):1–20

    Article  Google Scholar 

  • Wilens TE, Ritchie JC, Carroll BJ (1984) Comparison of plasma cortisol and corticosterone in the dexamethasone suppression test for melancholia. Psychoneuroendocrinology 9(1):45–55

    Article  CAS  PubMed  Google Scholar 

  • Wingfield JC (2005) The concept of allostasis: coping with a capricious environment. J Mammal 86(2):248–254

    Article  Google Scholar 

  • Zarkovic M, Ignjatovic S, Dajak M, Ciric J, Beleslin B, Savic S (2008) Cortisol response to ACTH stimulation correlates with blood interleukin 6 concentration in healthy humans. Euro J Endoc 159(5):649–652

    Article  CAS  Google Scholar 

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Acknowledgments

The authors also wish to thank Bente Sunde, Steinar Johnsen and Roald Jakobsen at the University of Nordland, Faculty of Biosciences and Aquaculture for providing assistance and support during the experiments. Additional thanks to Hege Iversen Haugmo for editing of all version of the manuscript. The experiment described has been approved by the local responsible laboratory animal science specialist under the surveillance of the Norwegian Animal Research Authority (NARA) and registered by the Authority.

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  1. Faculty of Biosciences and Aquaculture, University of Nordland, 8049, Bodø, Norway

    Martin H. Iversen & Robert A. Eliassen

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  1. Martin H. Iversen
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Correspondence to Martin H. Iversen.

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Iversen, M.H., Eliassen, R.A. The effect of allostatic load on hypothalamic–pituitary–interrenal (HPI) axis before and after secondary vaccination in Atlantic salmon postsmolts (Salmo salar L.). Fish Physiol Biochem 40, 527–538 (2014). https://doi.org/10.1007/s10695-013-9863-x

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