Protective Effects of Ectoine on Physiological Parameters of Daphnia Magna Subjected to Clove Oil-Induced Anaesthesia

Clove oil (CO) used as an anaesthetic in aquaculture causes toxic effects in fish and invertebrates since it has a narrow margin between effective and lethal concentrations. Ectoine (ECT) is an osmoprotectant produced by halophilic bacteria in response to stressful factors. It was hypothesized that ECT may attenuate physiological alterations induced by CO in aquatic animals. The aim of the present study was to determine if ECT induces protective effects in Daphnia magna subjected to COinduced anaesthesia. Daphnids were treated with 50 or 150 µL/L CO alone or in the combination with 10, 25 or 50 mg/L ECT. The results showed that both concentrations of CO alone induced anaesthesia, heart arrhythmia, decreased heart rate, increased diastole/systole ratio and duration of diastole. On the other hand, ECT attenuated alterations evoked by CO with the most significant effects in the combination of 50 µL/L CO+25 mg/L ECT. The animals showed a prolonged TtA and attenuated depression of thoracic limb activity, heart rate, arrhythmia, decreased diastole/systole ratio and duration of diastole. The results indicate that ECT may be a cardioprotective agent in anaesthesized crustaceans.

PDF

___

Akbari, S., Khoshnod, M.J., Rajaian, H., Afsharnasab, M. 2010. The use of eugenol as an anesthetic in transportation of with indian shrimp (Fenneropenaeusindicus) post larvae. Turkish Journal of Fisheries and Aquatic Sciences, 10: 423-429. DOI: 10.4194/trjfas.2010.0317

American Society of Testing and Materials Standard practice for conducting static acute toxicity tests on wastewaters with Daphnia: Annual book of ASTM standards. 1986, Vol. 11.04. Philadelphia, D4229- D4284.

Arina, B, Iqbal, A. 2002. In vitrofungitoxicity of the essential oil of Syzygiumaromaticum. World Journal of Microbiology and Biotechnology, 18: 317-319. DOI: 10.1023/A:1015242901360

Barbosa, I.R., Martins, R.M., Sa e Melo, M.L., Soares, A.M.V.M. 2003. Acute and chronic toxicity of dimethylsulfoxide to Daphnia magna. Bulletn of Environmental Contamination. Toxicology, 70: 1264- 1268. DOI: 10.1007/s00128-003-0119-9

Bekker, J.M., Krijgsman, B.J. 1951. Physiological investigations into the heart function of Daphnia. Journal of Physiology, 115: 249-257.

Berthoud, M.C., Reilly, C.S. 1992. Adverse effects of general anaesthetics. Drug Safety, 7: 434-459. DOI: 10.2165/00002018-199207060-00005

Birdsall, T.C. 1998. Therapeutic applications of taurine. Alternative Medicine Reviews, 3: 128-136.

Boudoulas, H., Rittgers, S.E., Lewis, R.P., Leier, C.V, Weissler, A.M. 1979. Changes in diastolic time with various pharmacologic agents: implication for myocardial perfusion. Circulation. 60, 164-169. DOI: 10.1161/01.CIR.60.1.164

Bownik, A. 2015. Clove essential oil from eugeniacaryophyllus induces anesthesia, alters swimming performance, heart functioning and decreases survival rate during recovery of Daphnia magna. Turkish Journal of Fisheries and Aquatic Sciences, 15: 157-166.

Bownik, A., St?pniewska, Z., Skowro?ski, T. 2015. Effects of ectoine of behavioural, physiological and biochemical parameters of Daphnia magna. Comparative Biochemistry and Physiology. Part C: Toxicology and Pharmacology, 168: 2-10. DOI: 10.1016/j.cbpc.2014.11.001

Bownik, A., St?pniewska, Z., Skowro?ski, T. 2014. Protective effects of ectoine in heat-stressed Daphniamagna. Journal of Comparative Physiology, 184: 961- 976. DOI: 10.1007/s00360-014-0860-x

Boyer S.E., White J.S., Stier A.C., Osenberg C.W. 2009. Effects of the fishanesthetic, clove oil (eugenol), on coral health and growth. Journal of Experimental Marine Biology and Ecology, 369: 53-57. DOI:10.1016/j.jembe.2008.10.020

Campbell, A.K., Wann, K.T., Matthews, S.B. 2004. Lactose causes heart arrhythmia in the water flea Daphnia pulex. Comparative Biochemistry and Physiology Part B, 139: 225-234. DOI:10.1016/j.cbpc.2004.07.004

Chaieb, K., Zmantar, T., Ksouri, R., Hajlaoui, H., Mahdouani, K., Abdelly, C., Bakhrouf, A. 2007. Antioxidant properties of essential oil of Eugeniacaryophyllata and its antifungal activity against a large number of clinical Candida species. Mycoses, 50: 403-406. DOI: 10.1111/j.1439-0507.2007.01391.x

Cho, J.S., Kim, T.H., Lim, J.M., Song, J.H. 2008. Effects of eugenol on Na+ currents in rat dorsal root ganglion neurons. Brain Research, 1243: 53-62. DOI: 10.1016/j.brainres.2008.09.030.

Chung, G., Rhee, J.N., Jung, S.J., Kim, J.S., Oh, S.B. 2008. Modulation of CaV2.3 calcium channel currents by eugenol. Journal of Dental Research, 87: 137-141. DOI: 10.1177/154405910808700201

da Costa, M.S., Santos, H., Galinski, E.A. 1998. An overview of the role and diversity of compatible solutes in Bacteria and Archaea. Advances in Biochemistry Engeneering and Biotechnology, 61: 117-153. DOI: 10.1007/BFb0102291

Damiani, C.E.N., Rossoni, L.V., Vassallo, D.V. 2003. Vasorelaxant effects of eugenol on rat thoracic aorta. Vascular Pharmacology, 40: 59- 66. DOI: 10.1016/S1537-1891(02)00311-7

Dobre, A.A., Gagiu, V., Petru, N. 2011. Antimicrobial activity of essential oils against food-borne bacteria evaluated by two perliminary methods. Romanian Biotechnology Letters, 16: 119-125.

Dyson, D.H., Maxie, M.G., Schnurr, D. 1998. Morbidity and mortality associated with anesthetic management in small animal veterinary practice in Ontario. Journal of American Animal Hospital Association. 34: 325- 335.

Eby, G., Halcomb, W.W. 2006. Elimination of cardiac arrhythmias using oral taurine with l-arginine withcase histories: Hypothesis for nitric oxide stabilization of the sinus node. Medical Hypotheses. 67: 1200- 1204. DOI:http://dx.doi.org/10.1016/j.mehy.2006.04.055

Fu, Y., Zu, Y., Chen, L., Shi, X., Wang, Z., Sun, S., Efferth, T. 2007. Antimicrobial activity of clove and rosemary essential oils alone and in combination. Phytotherapy Research, 21: 989-994. DOI: 10.1002/ptr.2179

Galinski, E.A., Pfeiffer, H.P., Truper, H.G. 1985. 1, 4, 5, 6- Tetrahydro-2-methyl-4-pyrimidinecarboxylic acid. A novel cyclic amino acid from halophilic phototrophic bacteria of the genus Ectothiorhodospira. European Journal of Biochemistry, 149: 135-139. DOI: 10.1111/j.1432-1033.1985.tb08903.x

Hamackova, J., Kouril, J., Kozak, P., Stupka, Z. 2006. Clove oil as an an anaesthetic for different freshwaterfish species. Bulgarian Journal of Agricultural Sciences, 12: 185-194.

Hill, J.V., Forster, M.E. 2004. Cardiovascular responses of Chinook salmon (Oncorhynchustshawytscha) during rapid anaesthetic induction and recovery. Comparative Biochemistry and Physiology. C, 137: 167-177. DOI: 10.1016/j.cca.2004.01.002

Huang, C.W., Chow, J.C., Tsai, J.J., Wu, SN. 2012. Characterizing the effects of eugenol on neuronal ionic currents and hyperexcitability. Psychopharmacology (Berlin). 221: 575-587. DOI:10.1007/s00213-011-2603-y

Isaacs, G. 1983. Permanent local anaesthesia and anhydrosis after clove oil spillage. Lancet, 1: 882-883. DOI: http://dx.doi.org/10.1016/S0140-6736(83)91428-9.

Jaganathan, S.K., Mazumdar, A., Mondhe, D., Mandal, M. 2011. Apoptotic effect of eugenol in human colon cancer cell lines. Cell Biology International, 35: 607- 615. DOI: 10.1042/CBI20100118

Javahery, S., Nekoubin, H., Moradlu, A.H. 2012. Effects of anaesthesia with clove oil in fish (review). Fish Physiology and Biochemistry, 38: 1545-1552. DOI: 10.1007/s10695-012-9682-5

Kalra, S. and Hayaran N. 2011. Arrhythmias following spinal anesthesia for cesarean delivery - Is Wenckebach common? Journal of Anaesthesiology and Clinical Pharmacology. 27: 541-543. DOI:10.4103/0970-9185.86604

Katz, A.M., Lorell, B.H. 2000. Regulation of cardiac contraction and relaxation. Circulation, 102: Iv-69-Iv- 74. DOI:10.1161/01.CIR.102.suppl_4.IV-69.

Kuner, J., Enescu, V., Utsu, F., Boszormenyi, E., Bernstein, H., Corday, E. 1967. Cardiac arrhythmias during anesthesia. 52: 580-587. DOI:10.1378/chest.52.5.580

Lahlou, S., Interaminense, L.F., Magalhães, P.J., LealCardoso, J.H., Duarte, G.P. 2004. Cardiovascular effects of eugenol, a phenolic compound present in many plant essential oils, in normotensive rats. Journal of Cardiovascular Pharmacology, 43: 250- 257.

Lippert, K., Galinski, E.A. 1992. Enzyme stabilization by ectoine-type compatible solutes: protection against heating, freezing and drying. Applied Microbiology and Biotechnology, 37: 61-65. DOI: 10.1007/BF00174204

Lovern, S.B., Strickler, J.R., Klaper, R. 2007. Behavioral and physiological changes in Daphnia magna when exposed to nanoparticle suspensions (titanum dioxide, nano-C60 and C60HxC70Hx). Environmental Science and Technology 41: 4465-4470. DOI: 10.1021/es062146p

McCowley, E.L. 1955. Management of cardiac arrhythmias during anaesthesia. Canadian Anaesthesia Society. 2: 137-141. DOI: 10.1007/BF03021107

McKenzie, J.D., Calow, P., Clyde, J., Miles, A., Dickinson, R., Lieb, W.R., Franks, N.P. 1992. Effects of temperature on the anaesthetic potency of halothane, enflurane and ethanol in Daphnia magna (Cladocera: Crustacea). Comparative Biochemistry and Physiology, C, 101: 15-19. DOI:10.1016/0742- 8413(92)90193-B

McKenzie, J.D., Calow, P., Nimmo, W.S. 1989. A model to test the potency of inhalation anaesthetics. British Journal of Anaesthesia, 63: 489-91. DOI: 10.1093/bja/63.4.489

Mitchell, M.A., Riggs, S.M., Singleton, C.B. Diaz-Figueroa, O.D., Hale, L.K. 2009. Evaluating the clinical and cardiopulmonary effects of clove oil and propofol in tiger salamanders (Ambystomatigriunum). Journal of Exotic Pet Medicine, 1: 50-56. DOI:10.1053/j.jepm.2008.11.001

Nagata, S., Wang,Y.B. 2001. Accumulation of ectoine in the halotolerantbrevibacterium sp. JCM6894. Journal of Bioscience and Bioengeneering, 91: 288-293. DOI: 10.1016/S1389-1723(01)80136-5

Norton, J.H., Dashorst, M., Lansky, T.M., Mayer, R.J. 1996. An evaluation of some relaxants for use with pearl oysters. Aquaculture.144: 39-52. http://www.epa.gov/pesticides/biopesticides/ingredien ts/factsheets/factsheet_florals.htm

Okushima, S., Vettorato, E., Corletto, F. 2014. Chronotropic effect of propofol or alfaxalone following fentanyl administration in healthy dogs. Veterinary Anaesthesia and Analgesia. 4: [Epub]. DOI: http://dx.doi.org/10.1111/vaa.12166

Parodi, T.V., Cunha, M.A., Heldwein, C.G., de Souza, D.M., Martins, Á.C., Garcia, Lde O., Wasielesky, W. Jr., Monserrat, J.M., Schmidt, D., Caron, B.O., Heinzmann, B., Baldisserotto, B. 2012. The anesthetic efficacy of eugenol and the essential oils of Lippia alba and Aloysiatriphylla in post-larvae and sub-adults of Litopenaeusvannamei (Crustacea, Penaeidae). Comparative Biochemistry and Physiology C. Toxicology and Pharmacology, 155: 462-468. DOI: 10.1016/j.cbpc.2011.12.003. Epub 2011 Dec 16.

Pastor, J., Salvador, M., Argandoña, M., Bernal, V., ReinaBueno, M., Csonka, L., et al. 2010. Ectoines in cell stress protection: uses and biotechnological production. Biotechnology Advances, 28: 782-801. DOI: 10.1016/j.biotechadv.2010.06.005

Pastor, J.M., Bernal, V., Salvador, M., Argandoña, M., Vargas, C., Csonka, L., Sevilla, Á., Iborra, J. L., Nieto, J. J. and Cánovas M. 2013. Role of central metabolism in the osmoadaptation of the halophilic bacterium Chromohalobactersalexigens. Journal of Biology and Chemistry, 288: 17769-17781. DOI: 10.1074/jbc.M113.470567

Pirow, R., Wollinger, R., Paul, R.J. 1999. The importance of the feeding current for oxygen uptake in the water flea Daphnia magna. Journal of Experimental Biology, 202: 553-562.

Postmes, T.J., Prick, R., Brorens, I. 1989. The deceleration of the heart frequency in the waterfleaDaphnia magna by adrenoceptor agonists and antagonists. Hydrobiologia, 171: 141-148. DOI: 10.1007/BF00008174

Prashar, A., Locke, I.C., Evans, C.S. 2006. Cytotoxicity of clove (Syzygiumaromaticum) oil and its major components to human skin cells. Cell Prolifation, 39: 241-248. DOI: 10.1111/j.1365-2184.2006.00384.x

Rana, I.S., Rana, A.S., Rajak, R.C. 2011. Evaluation of antifungal activity in essential oil of the Syzygiumaromaticum (L.) by extraction, purification and analysis of its main component eugenol. Brazilian Journal of Microbiology 42: 1269- 1277. DOI: 10.1590/S1517 83822011000400004

Roessler, M., Müller, V. 2001. Osmoadaptation in Bacteria and Archaea: common principles and differences. Environmental Microbiology , 3: 743-754. DOI: 10.1074/jbc.M113.470567

Satoh, H. 1994. Cardioprotective actions of taurine against intracellular and extracellular calcium-induced effects. Huxtable et al., (eds.) Taurine in Health and Disease. Springer, New York.

Sladky, K.K., Swanson C.R., Stoskopf M.K., Loomis M.R., Lewbart G.A. 2001. Comparative efficacy of tricainemethanesulfonate and clove oil for use as anesthetics in red pacu (Piaractusbrachypomis). American Journal of Veterinary Research, 62: 337- 342. DOI: 10.2460/ajvr.2001.62.337

Stein, R.J., Richter, W.R., Zussman, R.A., Brynjolfsson G. 1966. Ultrastructural characterization of Daphnia heart muscle. Journal of Cell. Biology, 29: 168-170. DOI:10.1083/jcb.29.1.168

US EPA. Floral Attractants, Repellents, and Insecticides. 2004 US Environmental Protection Agency. Venarsky, M.P., Vilhelm, F.M. 2006. Use of clove oil to anesthesize freshwater amphipods. Hydrobiologia, 568: 425-432. DOI: 10.1007/s10750-006-0225-x

Villegas-Navarro, A., Rosas-L.E., Reyes, J.L. 2003. The heart of Daphnia magna: effects of four cardioactive drugs. Comparative Biochemistry and Physiology,Part C 136: 127-134. DOI:10.1016/S1532- 0456(03)00172-8

Wei, Y.H., Yuan, F.W., Chen, W.C., Chen, S.Y. 2011. Production and characterization of ectoine by Marinococcussp. ECT1 isolated from a high-salinity environment. Journal of Bioscience and Bioengeneering, 111: 336-342. DOI:10.1016/j.jbiosc.2010.11.009.

Xu,Y-J., Arneja, A.S., Tappia, P.S., Dhalla, N.S. 2008.The potential health benefits of taurine in cardiovascular disease. Experimental and Clinical Cardiology, 13: 57-65.