Abstract
Stress in response to anesthesia with benzocaine, MS-222, metomidate and isoeugenol was studied in Atlantic salmon (Salmo salar), Atlantic halibut (Hippoglossus hippoglossus), and Atlantic cod (Gadus morhua) with no concomitant stress from handling or confinement in association with anesthesia or sampling. All of the anesthetics tested induced a stress response in all species, displayed by a release of cortisol to the water. MS-222 anesthesia elicited the highest cortisol release rates, reaching maximum levels 0.5 h post-exposure and returning to basal levels after 3–4 h. Benzocaine anesthesia caused a bimodal response where the initial peak in cortisol release rate was followed by a second increase lasting towards the end of the trial (6 h). This bimodality was more profound in Atlantic salmon than in Atlantic halibut and Atlantic cod. Metomidate anesthesia induced the lowest release of cortisol of the agents tested in both Atlantic halibut and Atlantic cod, but resulted in a bimodal response in Atlantic salmon where the initial increase in cortisol release was followed by a larger increase peaking at 2–2.5 h post exposure before returning to basal levels after 5 h. The stress induced in Atlantic salmon by isoeugenol anesthesia resembled that of MS-222, but did not reach the same elevated level. Overall, the cortisol release was most profound in Atlantic salmon followed by Atlantic halibut and Atlantic cod.
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Ackerman PA, Morgan JD, Iwama GK (2005) Anesthetics. CCAC guidelines on: the care and use of fish in research, teaching and testing. Canadian Council on Animal Care, Ottawa. Available at: http://www.ccac.ca/en/CCAC_Programs/Guidelines_Policies/GDLINES/Fish/Fish%20Anesthetics%20-%20ENG.pdf Accessed 10 Feb 2009
Aoshima H, Hamamoto K (1999) Potentiation of GABAA receptors expressed in Xenopus oocytes by perfume and phytoncid. Biosci Biotechnol Biochem 63:743–748
Ashton D, Wauquier A (1985) Modulation of a GABA-ergic inhibitory circuit in the in vitro hippocampus by etomidate isomers. Anesth Analg 64:975–980
Barton BA (2000) Salmonid fishes differ in their cortisol and glucose responses to handling and transport stress. N Am J Aquac 62:12–18
Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integ Comp Biol 42:517–525
Barton BA, Iwama GK (1991) Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Annu Rev Fish Dis 1:3–26
Barton BA, Peter RE (1982) Plasma cortisol stress response in fingerling rainbow trout, Salmo gairdneri Richardson, to various transport conditions, anaesthesia, and cold shock. J Fish Biol 20:39–51
Cho GK, Heath DD (2000) Comparison of tricaine methanesulphonate (MS222) and clove oil anaesthesia effects on the physiology of juvenile Chinook salmon Oncorhynchus tshawytscha (Walbaum). Aquac Res 31:537–546
Davidson GW, Davie PS, Young G, Fowler RT (2000) Physiological responses of rainbow trout Oncorhynchus mykiss to crowding and anesthesia with AQUI-S™. J World Aquac Soc 31:105–114
Davis KB (2006) Management of physiological stress in finfish aquaculture. N Am J Aquac 68:116–121
Davis KB, Griffin BR (2004) Physiological responses of hybrid striped bass under sedation by several anesthetics. Aquaculture 233:531–548
Davis KB, Parker NC, Suttle MA (1982) Plasma corticosteroids and chlorides in striped bass exposed to tricaine methanesulfonate, quinaldine, etomidate, and salt. Prog Fish-Cult 44:205–207
Donaldson EM (1981) The pituitary-interrenal axis as an indicator of stress in fish. In: Pickering AD (ed) Stress and Fish. Academic, London, pp 11–47
Eliason EJ, Kiessling A, Karlsson A, Djordjevic B, Farrell AP (2007) Validation of the hepatic portal vein cannulation technique using Atlantic salmon Salmo salar L. J Fish Biol 71:290–297
Ellis T, James JD, Stewart C, Scott AP (2004) A non-invasive stress assay based upon measurement of free cortisol released into the water by rainbow trout. J Fish Biol 65:1233–1252
Ellis T, James JD, Sundh H, Fridell F, Sundell K, Scott AP (2007) Non-invasive measurement of cortisol and melatonin in tanks stocked with seawater Atlantic salmon. Aquaculture 272:698–706
Fanouraki E, Papandroulakis N, Ellis T, Mylonas CC, Scott AP, Pavlidis M (2008) Water cortisol is a reliable indicator of stress in European sea bass, Dicentrarchus labrax. Behaviour 145:1267–1281
Frazier DT, Narahashi T (1975) Tricaine (MS-222): effects on ionic conductances of squid axon membranes. Eur J Pharmacol 33:313–317
Grasshoff C, Drexler B, Rudolph U, Antkowiak B (2006) Anaesthetic drugs: linking molecular actions to clinical effects. Curr Pharm Des 12:3665–3679
Greenwood LN, Scott AP, Vermerissen ELM, Mylonas CC, Pavlidis M (2001) Plasma steroids in mature common dentex (Dentex dentex) stimulated with a gonadotropin-releasing hormone agonist. Gen Comp Endocrinol 123:1–12
Hunn JB, Allen JL (1974) Movement of drugs across gills of fishes. Annu Rev Pharmacol Toxicol 14:47–55
Iversen M, Finstad B, McKinley RS, Eliassen RA (2003) The efficacy of metomidate, clove oil, Aqui-S™ and Benzoak® as anaesthetics in Atlantic salmon (Salmo salar L.) smolts, and their potential stress-reducing capacity. Aquaculture 221:549–566
Jentoft S, Aastveit AH, Torjesen PA, Andersen O (2005) Effects of stress on growth, cortisol and glucose levels in non-domesticated Eurasian perch (Perca fluviatilis) and domesticated rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol A 141:353–358
Kiessling A, Johansson D, Zahl IH, Samuelsen OB (2009) Pharmacokinetics, plasma cortisol and effectiveness of benzocaine, MS-222 and isoeugenol measured in individual dorsal aorta-cannulated Atlantic salmon (Salmo salar) following bath administration. Aquaculture 286:301–308
King WV, Hooper B, Hillsgrove S, Benton C, Berlinsky DL (2005) The use of clove oil, metomidate, tricaine methanesulphonate and 2-phenoxyethanol for inducing anaesthesia and their effect on the cortisol stress response in black sea bass (Centropristis striata L.). Aquac Res 36:1442–1449
King WV, Buckley LJ, Berlinsky DL (2006) Effect of acclimation temperature on the acute stress response in juvenile Atlantic cod, Gadus morhua L., and haddock, Melanogrammus aeglefinus L. Aquac Res 37:1685–1693
Kreiberg H, Powell J (1991) Metomidate sedation reduces handling stress in chinook salmon. World Aquac 22:58–59
Lee MH, Yeon KY, Park CK, Li HY, Fang Z, Kim MS, Choi SY, Lee SJ, Lee S, Park K, Lee JH, Kim JS, Oh SB (2005) Eugenol inhibits calcium currents in dental afferent neurons. J Dent Res 84:848–851
Li HY, Park CK, Jung SJ, Choi SY, Lee SJ, Park K, Kim JS, Oh SB (2007) Eugenol inhibits K+ currents in trigeminal ganglion neurons. J Dent Res 86:898–902
Maule AG, Tripp RA, Kaattari SL, Schreck CB (1989) Stress alters immune function and disease resistance in chinook salmon (Oncorhynchus tshawytscha). J Endocrinol 120:135–142
Mazeaud MM, Mazeaud F (1981) Adrenergic responses to stress in fish. In: Pickering AD (ed) Stress and Fish. Academic, London, pp 49–75
Molinero A, Gonzalez J (1995) Comparative effects of MS 222 and 2-phenoxyethanol on gilthead sea bream (Sparus aurata L) during confinement. Comp Biochem Physiol A 111:405–414
Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268
Neumcke B, Schwarz W, Stampfli R (1981) Block of Na channels in the membrane of myelinated nerve by benzocaine. Pflugers Arch 390:230–236
Olsen YA, Einarsdottir IE, Nilssen KJ (1995) Metomidate anesthesia in Atlantic salmon, Salmo salar, prevents plasma cortisol increase during stress. Aquaculture 134:155–168
Olsen RE, Sundell K, Hansen T, Hemre GI, Myklebust R, Mayhew TM, Ringo E (2002) Acute stress alters the intestinal lining of Atlantic salmon, Salmo salar L.: an electron microscopical study. Fish Physiol Biochem 26:211–221
Olsen RE, Sundell K, Ringo E, Myklebust R, Hemre GI, Hansen T, Karlsen O (2008) The acute stress response in fed and food deprived Atlantic cod, Gadus morhua L. Aquaculture 280:232–241
Oyama T (1973) Endocrine responses to anesthetic agents. Br J Anaesth 45:276–281
Oyama T, Wakayama S (1988) The endocrine responses to general anesthesia. Int Anesthesiol Clin 26:176–181
Park CK, Li HY, Yeon KY, Jung SJ, Choi SY, Lee SJ, Lee S, Park K, Kim JS, Oh SB (2006) Eugenol inhibits sodium currents in dental afferent neurons. J Dent Res 85:900–904
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
Pottinger TG, Moran TA (1993) Differences in plasma cortisol and cortisone dynamics during stress in two strains of rainbow trout (Oncorhynchus mykiss). J Fish Biol 43:121–130
Pottinger TG, Moran TA, Morgan JAW (1994) Primary and secondary indices of stress in the progeny of rainbow trout (Oncorhynchus mykiss) selected for high and low responsiveness to stress. J Fish Biol 44:149–163
Rang HP, Dale MM, Ritter JM, Moore PK (2003) Pharmacology. Churchill Livingstone, London
Reid SG, Bernier NJ, Perry SF (1998) The adrenergic stress response in fish: control of catecholamine storage and release. Comp Biochem Physiol C 120:1–27
Ross LG, Ross B (2008) Anaesthetic and sedative techniques for aquatic animals. Blackwell Publishing, Oxford
Rusch D, Zhong HJ, Forman SA (2004) Gating allosterism at a single class of etomidate sites on α1β2γ2L GABAA receptors accounts for both direct activation and agonist modulation. J Biol Chem 279:20982–20992
Sandodden R, Finstad B, Iversen M (2001) Transport stress in Atlantic salmon (Salmo salar L.): anaesthesia and recovery. Aquac Res 32:87–90
Scott AP, Ellis T (2007) Measurement of fish steroids in water—a review. Gen Comp Endocrinol 153:392–400
Scott AP, Hirschenhauser K, Bender N, Oliveira R, Earley RL, Sebire M, Ellis T, Pavlidis M, Hubbard PC, Huertas M, Canario A (2008) Non-invasive measurement of steroids in fish-holding water: important considerations when applying the procedure to behaviour studies. Behaviour 145:1307–1328
Sink TD, Strange RJ, Sawyers RE (2007) Clove oil used at lower concentrations is less effective than MS-222 at reducing cortisol stress responses in anesthetized rainbow trout. N Am J Fish Manage 27:156–161
Small BC (2003) Anesthetic efficacy of metomidate and comparison of plasma cortisol responses to tricaine methanesulfonate, quinaldine and clove oil anesthetized channel catfish Ictalurus punctatus. Aquaculture 218:177–185
Small BC (2004) Effect of isoeugenol sedation on plasma cortisol, glucose, and lactate dynamics in channel catfish Ictalurus punctatus exposed to three stressors. Aquaculture 238:469–481
Small BC, Chatakondi N (2005) Routine measures of stress are reduced in mature channel catfish during and after AQUI-S anesthesia and recovery. N Am J Aquac 67:72–78
Sorensen PW, Scott AP (1994) The evolution of hormonal sex-pheromones in teleost fish–poor correlation between the pattern of steroid release by goldfish and olfactory sensitivity suggests that these cues evolved as a result of chemical spying rather than signal specialization. Acta Physiol Scand 152:191–205
Sumpter JP, Dye HM, Benfey TJ (1986) The effects of stress on plasma ACTH, α-MSH, and cortisol levels in salmonid fishes. Gen Comp Endocrinol 62:377–385
Thomas P, Robertson L (1991) Plasma-cortisol and glucose stress responses of red drum (Sciaenops ocellatus) to handling and shallow-water stressors and anesthesia with MS-222, quinaldine sulfate and metomidate. Aquaculture 96:69–86
Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625
Wie MB, Won MH, Lee KH, Shin JH, Lee JC, Suh HW, Song DK, Kim YH (1997) Eugenol protects neuronal cells from excitotoxic and oxidative injury in primary cortical cultures. Neurosci Lett 225:93–96
Yang J, Uchida I (1996) Mechanisms of etomidate potentiation of GABAA receptor-gated currents in cultured postnatal hippocampal neurons. Neuroscience 73:69–78
Zeller A, Arras M, Lazaris A, Jurd R, Rudolph U (2005) Distinct molecular targets for the central respiratory and cardiac actions of the general anesthetics etomidate and propofol. FASEB J 19:1677–1679
Acknowledgments
The authors would like to thank the staff of the Institute of Marine Research, and in particular Ivar Helge Matre and Rina Helen Skoglund for their valuable technical assistance, and Grethe Thorsheim for skilful help and support with water sample processing and analysis. Ole Folkedal and Thomas Torgersen are highly acknowledged for proficient support in calculating cortisol release rates. Financial support was given by the Norwegian Research Council, grant no. 152898/120.
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Zahl, I.H., Kiessling, A., Samuelsen, O.B. et al. Anesthesia induces stress in Atlantic salmon (Salmo salar), Atlantic cod (Gadus morhua) and Atlantic halibut (Hippoglossus hippoglossus). Fish Physiol Biochem 36, 719–730 (2010). https://doi.org/10.1007/s10695-009-9346-2
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DOI: https://doi.org/10.1007/s10695-009-9346-2