Investigating changes in some oxidative stress indicators in blood, mucus, brain, liver and gills of rainbow trout (Oncorhynchus mykiss) anesthetized with clove essential oil

Document Type : scientific research article

Authors

1 Corresponding Author, Dept. of Aquatic Sciences, Hamoun International Wetland Institute, Research Institute of Zabol, Zabol, Iran.

2 Dept. of Agronomy and Plant Breeding, Agriculture Institute, Research Institute of Zabol, Zabol, Iran

Abstract

The use of anesthesia is a common practice in aquaculture to sedate fish and mitigate handling stress. Although the employ of anesthesia is considered beneficial for fish, as it reduces stress and improves welfare, at the same time it may induce hazardous side-effects. The aim of the present study was to investigate anesthesia by clove (Eugenia cairyophillata) essential oil on oxidative stress parameters in rainbow trout (Oncorhynchus mykiss). In the first experiment, times of sedation, loss of equiblarium, induction, return of equiblarium and recovery from anesthesia were determined in the fish anesthetized with clove essential oil at the concentrations of 10, 25, 50, 75, 100 and ppm. In the second experiment, oxidative stress effects of clove essential oil were investigated in the fish after at 0 and 24 h after induction anesthesia. After induction of anesthesia, sampling of tissues (gill, brain, liver, blood and mucus) of 10 fish was done at 0 (10 minutes after anesthesia) and 24 hours after anesthesia. The samples were analyzed to evaluate the enzyme activity of superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPx). The results showed that anesthesia with clove essential oil did not cause significant changes in the activity of SOD and GPx enzymes in different tissues of fish. However, in some tissues, there were limited changes in the concentration of CAT enzyme due to anesthesia. Based on this, the concentration of 50 ppm of clove essential oil can be introduced as a suitable anesthetic in terms of not inducing oxidative stress in rainbow salmon. Considering that the changes in the concentrations of SOD, GPx and CAT in mucus and blood were mainly in line with the changes in other fish tissues (brain, liver and gills), non-invasive sampling (sampling of blood and mucus tissues) can be suggested to evaluate oxidative stress in fish anesthesia studies.

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1.Aydın, B., & Barbas, L. A. L. (2020). Sedative and anesthetic properties of essential oils and their active compounds in fish: A review. Aquaculture, 520, 734999.
2.Maricchiolo, G., & Genovese, L. (2011). Some contributions to knowledge of stress response in innovative species with particular focus on the use of the anaesthetics. The Open Marine Biology Journal, 5 (1), 24-33.
3.Javahery, S., Nekoubin, H., & Moradlu, A. H. (2012). Effect of anaesthesia with clove oil in fish. Fish physiology and biochemistry, 38, 1545-1552.
4.Khosravanizadeh, A., Rahdari, A., Pakzad Toochaei, S. (2023). Effect of 2-phenoxyethanol on antioxidant enzymes capacity in the various tissues of rainbow trout (Oncorhynchus mykiss). Iranian Scientific Fisheries Journal, 32 (2), 47-62.
5.Tubío, R. C., Weber, R. A., & Aldegunde, M. (2010). Home tank anesthesia: a very efficient method of attenuating handling stress in rainbow trout (Oncorhynchus mykiss, Walbaum). Journal of applied ichthyology, 26 (1), 116-117.
6.Cotter, P. A., & Rodnick, K. J. (2006). Differential effects of anesthetics on electrical properties of the rainbow trout (Oncorhynchus mykiss) heart. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 145 (2), 158-165.
7.Kazuń, K., & Siwicki, A. K. (2001). Propiscin–a safe new anaesthetic for fish. Fisheries & Aquatic Life, 9 (2), 183-190.
8.Munday, P. L., & Wilson, S. K. (1997). Comparative efficacy of clove oil and other chemicals in anaesthetization of Pomacentrus amboinensis, a coral reef fish. Journal of Fish Biology, 51 (5), 931-938.
9.Carrasco, S., Sumano, H., & Navarro-Fierro, R. (1984). The use of lidocaine-sodium bicarbonate as anaesthetic in fish. Aquaculture, 41 (4), 395-398.
10.Mylonas, C. C., Cardinaletti, G., Sigelaki, I., & Polzonetti-Magni, A. (2005). Comparative efficacy of clove oil and 2-phenoxyethanol as anesthetics in the aquaculture of European sea bass (Dicentrarchus labrax) and gilthead sea bream (Sparus aurata) at different temperatures. Aquaculture, 246 (1-4), 467-481.
11.Azad, I. S., Al-Yaqout, A., & Al-Roumi, M. (2014). Antibacterial and immunity enhancement properties of anaesthetic doses of thyme (Thymus vulgaris) oil and three other anaesthetics in Sparidentax hasta and Acanthopagrus latus. Journal of King Saud University-Science, 26 (2), 101-106.
12.Roohi, Z., & Imanpoor, M. R. (2015). The efficacy of the oils of spearmint and methyl salicylate as new anesthetics and their effect on glucose levels in common carp (Cyprinus carpio L., 1758) juveniles. Aquaculture, 437, 327-332.
13.Taheri Mirghaed, A., Ghelichpour, M., & Hoseini, S. M. (2016). Myrcene and linalool as new anesthetic and sedative agents in common carp, Cyprinus carpio- Comparison with eugenol. Aquaculture, 464, 165-170.
14.Cunha, J. A. D., Scheeren, C. Á., Salbego, J., Gressler, L. T., Madaloz, L. M., Bandeira-Junior, G., Bianchini, A. E., Pinheiro, C. G., Bordignon, S. A., Heinzmann, B. M., & Baldisserotto, B. (2017). Essential oils of Cunila galioides and Origanum majorana as anesthetics for Rhamdia quelen: efficacy and effects on ventilation and ionoregulation. Neotropical Ichthyology, 15, e160076.
15.Teixeira, R. R., de Souza, R. C., Sena, A. C., Baldisserotto, B., Heinzmann, B. M., Couto, R. D., & Copatti, C. E. (2017). Essential oil of Aloysia triphylla in Nile tilapia: anaesthesia, stress parameters and sensory evaluation of fillets. Aquaculture Research, 48 (7), 3383-3392.
16.Khosravanizadeh, A., Ghafari, M., Khajeh, M., Abtahi, B., Salehi, H., Zakipour Rahimabadi, E., & Ahmadipour Nezamabadi, K. (2012). Using clove oil (Eugenia caryophillata) loaded on the iron nanoparticles to induce anesthesia in Rainbow trout (Oncorhynchus mykiss). Iranian Scientific Fisheries Journal,20 (4), 43-52.
17.Rahdari, A., Khosravanizadeh, A., Dahmardeh, H., Gharaei, A., & Mirdar Harijani, J. (2017). Anesthetic effects and biochemical changes of peppermint essence (Mentha spicata) in snow
trout (Schizothorax zarudnyi). Aquatic Animals Nutrition, 3 (2), 35-46.
18.Rakhshani, M., Mirdar Harijani, J., & Gharaei, A. (2018). Investigating the anesthetic vigor and histopathological effects of Peppermint (Mentha piperita) essential oils in Common carp (Cyprinus carpio). Iranian Scientific Fisheries Journal, 27 (1), 1-10.
19.Golshan, N., Harijani, J. M., Gharaei, A., & Jamshidian, A. (2018). The effect of anesthetic Lavender (Lavendula officinalis) essential oil on histopathological and blood biochemical enzymes of silver carp (Hypophthalmichthys molitrix). Journal of Veterinary Research, 73 (1), 9-15.
20.Khosravanizadeh, A., Rahdari, A., & Gharaei, A. (2020). Anesthetic effects of Cuminum cyminum essential oil and 2-phenoxyethanol on zebrafish (Danio rario). Journal of Ornamental Aquatics, 7 (1), 17-25.
21.Sharifrohani, M., Haghighi, M., Asaeian, H., & Lashto Aghaei, Gh. (2008). A study of the anesthetic effect of Zataria multiflora Boiss (Labiatae) essence on Oncorhynchus mykiss
and cultured Salmo trutta caspius. Iranian Scientific Fisheries Journal, 16 (4), 99-106.
22.Sedigh Bazkiagourab, M., Sattari, M., & Imanpour Namin, J. (2021). Anesthetic effects of valerian extract (Valeriana officinalis), lemongrass extract (Cymbopogon citratus) and clove powder (Eugenia caryophyllata) on Sterlet sturgeon, (Acipenser ruthenus). Aquatic Physiology and Biotechnology, 9 (2), 59-86.
23.Eteghad, S., Ghavami, S., Mortazavi, J., & Mirzaei, H. (2008). Comparative survey on anesthetizing effects of medicinal herbs valerian officinalis, melissa officinalis, papaver somniferum, and papaver bracteatum on gold fish (Carassius auratus). Iranian Scientific Fisheries Journal, 17 (1), 91-98.
24.Nambiar, S. P., Banuru, S. C., Vahab, R. A., Ittoop, G., Nair, S. N., & Pillai, D. (2023). Augmentation of the anesthetic potency of clove oil for immersion anesthesia in fishes. Aquaculture International, 1-9.
25.Velisek, J., Stara, A., Li, Z. H., Silovska, S., & Turek, J. (2011). Comparison of the effects of four anaesthetics on blood biochemical profiles and oxidative stress biomarkers in rainbow trout. Aquaculture, 310 (3-4), 369-375.
26.Stringhetta, G. R., Barbas, L. A., Maltez, L. C., Sampaio, L. A., Monserrat, J. M., & Garcia, L. O. (2017). Oxidative stress responses of juvenile tambaqui Colossoma macropomum after short-term anesthesia with benzocaine and MS-222. Anais da Academia Brasileira de Ciências, 89, 2209-2218.
27.Azambuja, C. R., Mattiazzi, J., Riffel, A. P. K., Finamor, I. A., de Oliveira Garcia, L., Heldwein, C. G., ... & Llesuy, S. F. (2011). Effect of the essential oil of Lippia alba on oxidative stress parameters in silver catfish (Rhamdia quelen) subjected to transport. Aquaculture, 319 (1-2), 156-161.
28.Belló, A. R. R., Fortes, E., Belló-Klein, A., Belló, A. A., Llesuy, S. F., Robaldo, R. B., & Bianchini, A. (2000). Lipid peroxidation induced by Clinostomum detruncatum in muscle of the freshwater fish Rhamdia quelen. Diseases of aquatic organisms, 42 (3), 233-236.
29.Tew, K. D., & Ronai, Z. E. (1999). GST function in drug and stress response. Drug Resistance Updates, 2 (3), 143-147.
30.Monserrat, J. M., Martínez, P. E., Geracitano, L. A., Amado, L. L., Martins, C. M. G., Pinho, G. L. L., Heinzmann, B. M., Baldisserotto, B., Pavanato, M. A., & Bianchini, A. (2007). Pollution biomarkers in estuarine animals: critical review and new perspectives. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 146 (1-2), 221-234.
31.Storey, K. B. (1996). Oxidative stress: animal adaptations in nature. Brazilian journal of medical and biological research, 29, 1715-1733.
32.Lushchak, V. I., Bagnyukova, T. V., Husak, V. V., Luzhna, L. I., Lushchak, V., & Storey, K. B. (2005). Hyperoxia results in transient oxidative stress and an adaptive response by antioxidant enzymes in goldfish tissues. The international journal of biochemistry & cell biology, 37 (8), 1670-1680.
33.Adel, M., Sadegh, A. B., Yeganeh, S., Movafagh, A. N., & Saoud, I. P. (2016). Anesthetic efficacy of clove oil, propofol, 2‐phenoxyethanol, and ketamine hydrochloride on Persian Sturgeon, Acipenser persicus, juveniles. Journal of the World Aquaculture Society, 47 (6), 812-819.
34.Velíšek, J., Svobodova, Z., & Piačková, V. (2005). Effects of clove oil anaesthesia on rainbow trout (Oncorhynchus mykiss). Acta Veterinaria Brno, 74 (1), 139-146.
35.Keene, J. L., Noakes, D. L. G., Moccia, R. D., & Soto, C. G. (1998). The efficacy of clove oil as an anaesthetic for rainbow trout, Oncorhynchus mykiss (Walbaum). Aquaculture Research, 29 (2), 89-101.
36.Gharaei, A., Khajeh, M., Khosravanizadeh, A., Mirdar, J., & Fadai, R. (2020). Fluctuation of biochemical, immunological, and antioxidant biomarkers in the blood of beluga (Huso huso) under effect of dietary ZnO and chitosan–ZnO NPs. Fish physiology and biochemistry, 46 (2), 547-561.
37.Ross, N. W., Firth, K. J., Wang, A., Burk,a J. F., & Jojnson, S. C. (2000). Changes in hydrolytic enzyme activities of Atlantic salmon (Salmo salar) skin mucus due to infection with the Salmon louse (Lepeophtheirus salmonis) and cortisol implantation. Disease of Aquatic Organisems, 41, 43-51.
38.Zelen, I., Mitrovic, M., Jurisic-Skevini, A., & Arsenijevic, S. (2010). Activity of SOD and Catalase and MDA content in seminal plasma of infertile patients. Med. Preg, LXIII (9-10), 624-629.
39.Barbaneagra, T., Cristica, M., Ciornea, E., & Manoliu, A. (2012). Influence of nutritive substrate and pH on catalase and peroxidase production in saprophytic fungus Rhizopus nigricans. Journal of Experimental and Molecular Biology, 13 (3), 71.
40.Andersen, H. R., Nielsen, J. B., Nielsen, F., & Grandjean, P. (1997). Antioxidative enzyme activities in human erythrocytes. Clinical chemistry, 43 (4), 562-568.
41.Marking, L. L., & Meyer, F. P. (1985). Are better fish anaesthects needed in fisheries? Fisheries, 10, 2-5.
42.Anderson, W. G., McKinley, R. S., & Colavecchia, M. (1997). The use of clove oil as an anesthetic for rainbow trout and its effects on swimming performance. North American Journal of Fisheries Management, 17 (2), 301-307.
43.Soltani, M., Omidbeigi, R., Rezvani, S., Mehrabi, M. R., & Chitsaz, H. (2001) study of anesthetic effects induced by clove flower (Eugenia caryophillata) on rainbow trout (Oncorhynchus mykiss) under various water quality conditions, Journal of Veterinary Research, 56 (4), 85-89.
44.Woolsey, J., Holcomb, M., & Ingermann, R. L. (2004). Effect of temperature on clove oil anesthesia in steelhead fry. North American Journal of Aquaculture, 66 (1), 35-41.
45.Hikasa, Y., Takase, K., Ogasawara, T., & Ogasawara, S. (1986). Anaesthesia and recovery with tricane methanesul phonate, eugenol and thiopental sodium in the carp (Cyprinus carpio). Japanese Journal of Veterinary Science, 48, 341-351.
46.Sonawane, U. D., & Kulkarni, G. N. (2001). Anaesthetic effects of clove oil and sodium bicarbonate on the fry of Liza parsia. Iranian Journal of Fisheries Sciences, 3 (2), 49-62.
47.Gressler, L. T., Riffel, A. P. K., Parodi, T. V., Saccol, E. M. H., Koakoski, G., da Costa, S. T., Pavanato, M.A., Heinzmann, B.M., Caron, B., Schmidt, D., & Baldisserotto, B. (2014). Silver catfish Rhamdia quelen immersion anaesthesia with essential oil of Aloysia triphylla (L'Hérit) Britton or tricaine methanesulfonate: effect on stress response and antioxidant status. Aquaculture research, 45 (6), 1061-1072.
48.Di Marco, P., Priori, A., Finoia, M. G., Petochi, T., Marino, G., Lemarie, G., Alexis, M., Alberti, A., & Macciantelli, D. (2008). Plasma total oxidant/ antioxidant status in Dicentrarchus labrax after exposure to experimental hypoxia, hyperoxia and hypercapnia. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 151 (1), S15.
49.Buzadzić, B., Spasić, M. B., Saicić, Z. S., Radojicić, R., & Petrović, V. M. (1992). Seasonal dependence of the activity of antioxidant defence enzymes in the ground squirrel (Citellus citellus): the effect of cold. Comparative Biochemistry and physiology. B, Comparative Biochemistry, 101 (4), 547-551.
50.Kanatt, S. R., Chander, R., & Sharma, A. (2007). Antioxidant potential of mint (Mentha spicata L.) in radiation-processed lamb meat. Food chemistry, 100 (2), 451-458.
51.Schauss, A. G., Wu, X., Prior, R. L., Ou, B., Huang, D., Owens, J., Agarwal, A., Jensen, G. S., Hart, A. N., & Shanbrom, E. (2006). Antioxidant capacity and other bioactivities of the freeze-dried Amazonian palm berry, Euterpe oleraceae mart. (acai). Journal of agricultural and food chemistry,
54 (22), 8604-8610.
52.Halliwell, B., & Chirico, S. (1993). Lipid peroxidation: its mechanism, measurement, and significance. The American journal of clinical nutrition, 57 (5), 715-725.
53.Gülçin, İ., Elmastaş, M., & Aboul-Enein, H. Y. (2012). Antioxidant activity of clove oil–A powerful antioxidant source. Arabian Journal of chemistry, 5 (4), 489-499.
54.Pietta, P. G. (2000). Flavonoids as antioxidants. Journal of natural products, 63 (7), 1035-1042.
55.Cheeseman, K. H., & Slater, T. F. (1993). An introduction to free radical biochemistry. British medical bulletin, 49 (3), 481-493.
56.Wang, W., Dong, H., Sun, Y., Sun, C., Duan, Y., Gu, Q., Li, Y., Xie, M., & Zhang, J. (2020). Immune and physiological responses of juvenile Chinese sea bass (Lateolabrax maculatus) to eugenol and tricaine methanesulfonate (MS-222) in gills. Aquaculture Reports, 18, 100554.
57.Priborsky, J., Stara, A., Rezabek, J., Zuskova, E., Lepic, P., & Velisek, J. (2015). Comparison of the effect of four anaesthetics on haematological profiles, oxidative stress and antioxidant enzymes in barbel (Barbus barbus). Neuroendocrinology Letters, 36 (1).
58.Zahran, E., Risha, E., & Rizk, A. (2021). Comparison propofol and eugenol anesthetics efficacy and effects on general health in Nile Tilapia. Aquaculture, 534, 736251.
59.Yen, G. C., & Duh, P. D. (1994). Scavenging effect of methanolic extracts of peanut hulls on free-radical and active-oxygen species. Journal of agricultural and food chemistry, 42 (3), 629-632.
60.Saccol, E. M., Toni, C., Pês, T. S., Ourique, G. M., Gressler, L. T., Silva, L. V., Mourão, R. H., Oliveira, R. B., Baldisserotto, B., & Pavanato, M. A. (2016). Anaesthetic and antioxidant effects of Myrcia sylvatica (G. Mey.) DC. and Curcuma longa L. essential oils on tambaqui (Colossoma macropomum). Aquaculture Research, 48 (5), 2012-2031.
61.Boaventura, T. P., Souza, C. F., Ferreira, A. L., Favero, G. C., Baldissera, M. D., Heinzmann, B. M., Baldisserotto, B., & Luz, R. K. (2020). Essential oil of Ocimum gratissimum (Linnaeus, 1753) as anesthetic for Lophiosilurus alexandri: induction, recovery, hematology, biochemistry and oxidative stress. Aquaculture, 529, 735676.
62.Ferreira, A. L., Favero, G. C., Boaventura, T. P., de Freitas Souza, C., Ferreira, N. S., Descovi, S. N., Baldisserotto, B., Heinzmann, B. M., & Luz, R. K. (2021). Essential oil of Ocimum gratissimum (Linnaeus, 1753): efficacy for anesthesia and transport of Oreochromis niloticus. Fish Physiology and Biochemistry, 47 (1), 135-152.
63.Teles, M., Oliveira, M., Jerez-Cepa, I., Franco-Martínez, L., Tvarijonaviciute, A., Tort, L., & Mancera, J. M. (2019). Transport and recovery of gilthead sea bream (Sparus aurata L.) sedated with clove oil and MS222: Effects on oxidative stress status. Frontiers in physiology, 10, 523.
64.Yousefi, M., Hoseini, S. M., Vatnikov, Y. A., Nikishov, A. A., & Kulikov, E. V. (2018). Thymol as a new anesthetic in common carp (Cyprinus carpio): Efficacy and physiological effects in comparison with eugenol. Aquaculture, 495, 376-383.
65.Uçar, A., Atamanalp, M., Cankaya, M., & Özdemir, H. (2013). Effects of anesthetic substances on some antioxidan enzyme activities of Trouts. Journal of Fisheries Sciences. 7 (2), 152.
66.Akgündüz, M. Ç., Çavuşoğlu, K., & Yalçın, E. (2020). The potential risk assessment of phenoxyethanol with a versatile model system. Scientific reports, 10 (1), 1209.
67.MacDonald‐Wicks, L. K., Wood, L. G., & Garg, M. L. (2006). Methodology for the determination of biological antioxidant capacity in vitro: a review. Journal of the Science of Food and Agriculture, 86 (13), 2046-2056.
68.Aoshima, H., Tsunoue, H., Koda, H., & Kiso, Y. (2004). Aging of whiskey increases 1, 1-diphenyl-2-picrylhydrazyl radical scavenging activity. Journal of agricultural and food chemistry, 52 (16), 5240-5244.