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Effect of lemon balm (Melissa officinalis) extract on growth performance, digestive and antioxidant enzyme activities, and immune responses in rainbow trout (Oncorhynchus mykiss)

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Abstract

This study was conducted to determine the effects of dietary supplementation of lemon balm (Melissa officinalis) aqueous methanolic extract on growth performance, blood parameters, digestive and antioxidant enzyme activities, and non-specific immune responses in rainbow trout (Oncorhynchus mykiss). Fish with an average weight of 23.03 ± 0.07 g were fed a diet supplemented with an aqueous methanolic extract of lemon balm at a dose of 0 (control), 0.1 (LB0.1), 0.5 (LB0.5), and 1 g kg−1 (LB1) for 75 days. The final weight, weight gain, and specific growth rate were observed to be significantly increased in LB0.5 and LB1 groups compared with that of the control. No differences were observed in feed conversion ratio values. WBC increased at the 45th day of the study in LB0.1 group. No differences were determined in RBC (P > 0.05). At the end of the study, lipase increased significantly in all experimental groups compared with the control. Pepsin was also elevated in LB0.5 and LB1 groups compared with the control. Increased trypsin was determined in LB1 group (P < 0.05). SOD activity increased at the end of the study in LB1 group (P < 0.05). CAT values had no differences compared with control. GR activity increased in all experimental groups compared with control. GPx improved in LB0.5 and LB1 groups significantly (P < 0.05). Lipid peroxidation was decreased in LB1 group compared with that of control, but this decrease was not significant (P < 0.05). Oxidative radical production and lysozyme activity significantly increased in LB1 group (P < 0.05). The highest MPO was determined in control group (P < 0.05). Current results suggest that lemon balm extract stimulates growth promoting antioxidant and immune responses in rainbow trout.

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References

  • Almabrok AA, Amhamed ID, Mohamed GA, Bilen S, Altief TAS (2018) Effect of Tilia tomentosa methanolic extract on growth performance, digestive enzyme activity, immune system and haematological indices of common carp (Cyprinus carpio). Marine Science and Technology Bulletin 7:12–20

    Google Scholar 

  • Altunoglu YC, Bilen S, Ulu F, Biswas G (2017) Immune responses to methanolic extract of black cumin (Nigella sativa) in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 67:103–109

    Google Scholar 

  • Amhamed ID, Mohamed GA, Almabrok AA, Altıef TAS, Bilen S (2018) Efficacy of dietary Chenopodium album extract on some health parameters, digestive enzymes and growth performance in juvenile Cyprinus carpio. Alınteri Journal of Agriculture Sciences 33:165–176

    Google Scholar 

  • Amooaghaie R (2011) Melissa officinalis: an important dietary source of phenolic compounds with high antioxidant capacity. Planta Med 77:1424–1424

    Google Scholar 

  • Awad E, Austin B (2010) Use of lupin, Lupinus perennis, mango, Mangifera indica, and stinging nettle, Urtica dioica, as feed additives to prevent Aeromonas hydrophila infection in rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 33:413–420

    CAS  PubMed  Google Scholar 

  • Bernfeld P (1955) Amylases, α and β. Methods Enzymol 1:149–158

    CAS  Google Scholar 

  • Bilen S, Bulut M (2010) Effects of Laurel (Laurus nobilis) on the non-specific immune responses of rainbow trout (Oncorhynchus mykiss, Walbaum). J Anim Vet Adv 9:1275–1279

    CAS  Google Scholar 

  • Bilen S, Bulut M, Bilen AM (2011) Immunostimulant effects of Cotinus coggyria on rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 30:451–455

    PubMed  Google Scholar 

  • Bilen S, Altunoglu YC, Ulu F, Biswas G (2016a) Innate immune and growth promoting responses to caper (Capparis spinosa) extract in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 57:206–212

    CAS  PubMed  Google Scholar 

  • Bilen S, Unal S, Guvensoy H (2016b) Effects of oyster mushroom (Pleurotus ostreatus) and nettle (Urtica dioica) methanolic extracts on immune responses and resistance to Aeromonas hydrophila in rainbow trout (Oncorhynchus mykiss). Aquaculture 454:90–94

    Google Scholar 

  • Bilen S, Ozkan O, Alagoz K, Ozdemir KY (2018) Effect of dill (Anethum graveolens) and garden cress (Lepidium sativum) dietary supplementation on growth performance, digestive enzyme activities and immune responses of juvenile common carp (Cyprinus carpio). Aquaculture 495:611–616

    CAS  Google Scholar 

  • Blaxhall P, Daisley K (1973) Routine haematological methods for use with fish blood. J Fish Biol 5:771–781

    Google Scholar 

  • Ciftci O, Ozdemir I, Tanyildizi S, Yildiz S, Oguzturk H (2011) Antioxidative effects of curcumin, β-myrcene and 1, 8-cineole against 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin-induced oxidative stress in rats liver. Toxicol Ind Health 27:447–453

    CAS  PubMed  Google Scholar 

  • Citarasu T (2010) Herbal biomedicines: a new opportunity for aquaculture industry. Aquacult Int 18:403–414

    Google Scholar 

  • Cosge B, Arif I, Gurbuz B (2009) GC/MS analysis of herbage essential oil from lemon balms (Melissa officinalis L.) grown in Turkey. J Appl Bio Sci:149–152

  • Dada AA (2015) Improvement of tilapia (Oreochromis niloticus Linnaeus, 1758) growth performance fed three commercial feed additives in diets. J Aquac Res Development 6:325

    Google Scholar 

  • Ellis A (1990) Lysozyme assays In: Stolen JS, Fletcher TC, Anderson DP, Roberson BS, van Muiswinkel WB (eds) Techniques in fish immunology, vol 1. SOS Publications, Fair Haven, pp 101–103 Worthington CC (1988) Worthington enzyme manual: enzymes and related biochemicals. Worthington Biochemical Corporation

  • Erlanger BF, Kokowsky N, Cohen W (1961) The preparation and properties of two new chromogenic substrates of trypsin. Arch Biochem Biophys 95:271–278

    CAS  Google Scholar 

  • Fang Y-Z, Yang S, Wu G (2002) Free radicals, antioxidants, and nutrition. Nutrition 18:872–879

    CAS  PubMed  Google Scholar 

  • FAO (2018) Food and Agriculture Organization. World Food Agriculture Statistical Pocketbook, FAO 255 p

    Google Scholar 

  • Furne M et al (2005) Digestive enzyme activities in Adriatic sturgeon Acipenser naccarii and rainbow trout Oncorhynchus mykiss. A comparative study. Aquaculture 250:391–398

    CAS  Google Scholar 

  • Ghayour N, Behnam RM, Afsharian M, Tehranipour M, Ghayour MB (2010) The protective effects of Melissa officinalis leaves usage on learning disorder induced by lead acetate administration during pre and postnatal periods in rats. Arak Med Uni J 13:97–104

    Google Scholar 

  • Giannenas I, Triantafillou E, Stavrakakis S, Margaroni M, Mavridis S, Steiner T, Karagouni E (2012) Assessment of dietary supplementation with carvacrol or thymol containing feed additives on performance, intestinal microbiota and antioxidant status of rainbow trout (Oncorhynchus mykiss). Aquaculture:350-353–3526-32

  • Haghighi M, Sharif Rohani M, Pourmoghim H, Samadi M, Tavoli M, Eslami M, Yusefi R (2017) Enhancement of immune responses of rainbow trout (Oncorhynchus mykiss) fed a diet supplemented with Aloe vera extract. Iran J Fish Sci 16:884–896

    Google Scholar 

  • Hisar O, Yildirim S, Aras HN, Gultepe N (2009) Changes in liver and kidney antioxidant enzyme activities in the rainbow trout (Oncorhynchus mykiss) exposed cadmium. Asian J Chem 21:3133–3137

    CAS  Google Scholar 

  • Hohmann J, Zupko I, Redei D, Csanyi M, Falkay G, Mathe I, Janicsak G (1999) Protective effects of the aerial parts of Salvia officinalis, Melissa officinalis and Lavandula angustifolia and their constituents against enzyme-dependent and enzyme-independent lipid peroxidation. Planta Med 65:576–578

    CAS  PubMed  Google Scholar 

  • Iqbal KJ et al (2016) Effect of different plant and animal origin (fishmeal) feeds on digestive enzyme activity and haematology of juvenile Labeo rohita. Pak J Zool 48:201–207

    CAS  Google Scholar 

  • Iskesen I, Saribulbul O, Cerrahoglu M, Var A, Nazli Y, Sirin H (2006) Trimetazidine reduces oxidative stress in cardiac surgery. Circ J 70:1169–1173

    CAS  PubMed  Google Scholar 

  • Lau D et al (2005) Myeloperoxidase mediates neutrophil activation by association with CD11b/CD18 integrins. Proc Natl Acad Sci 102:431–436

    CAS  PubMed  Google Scholar 

  • Lee JY, Gao Y (2012) Review of the application of garlic, Allium sativum, in aquaculture. J World Aquacult Soc 43:447–458

    Google Scholar 

  • Lević J, Markov S, Đuragić O, Sredanović S (2008) Herbs and organic acids as an alternative for antibiotic-growth-promoters. In: 5th International Symposium of IBNA (National Research. Development Institute for Animal Biology and Nutrition), Balotesti, Bukurest. pp 28–29

  • Lewis S, Bain B, Bates I (2001) Dacie and Lewis practical haematology. Churchill Livingstone, New York

    Google Scholar 

  • Madhuri S, Mandloi A, Govind P, Sahni Y (2012) Antimicrobial activity of some medicinal plants against fish pathogens. Int Res J Phar 3:28–30

    Google Scholar 

  • Mazzanti G, Battinelli L, Pompeo C, Serrilli AM, Rossi R, Sauzullo I, Mengoni F, Vullo V (2008) Inhibitory activity of Melissa officinalis L. extract on herpes simplex virus type 2 replication. Nat Prod Res 22:1433–1440

    CAS  PubMed  Google Scholar 

  • Mohamadi Saei M, Beiranvand K, Khalesi MK, Mehrabi F (2016) Effects of dietary savory and myrtle essential oils on growth, survival, nutritional indices, serum biochemistry, and hematology of farmed rainbow trout, Oncorhynchus mykiss, fry. J World Aquacult Soc 47:779–785

    CAS  Google Scholar 

  • Mohamed GA, Amhamed ID, Almabrok AA, Barka ABA, Bilen S, Elbishti RT (2018) Effect of celery (Apium graveolens) extract on the growth, haematology, immune response and digestive enzyme activity of common carp (Cyprinus carpio). Marine Science and Technology Bulletin 7:51–59

    Google Scholar 

  • Oniga I, Vlase L, Toiu A, Benedec D, Duda M (2010) Evaluation of phenolic acid derivatives and essential oil content in some Melissa Officinalis L. Varieties Farmacia 58:764–769

    CAS  Google Scholar 

  • Platel K, Rao A, Saraswathi G, Srinivasan K (2002) Digestive stimulant action of three Indian spice mixes in experimental rats. Food/Nahrung 46:394–398

    PubMed  Google Scholar 

  • Ricker WE (1979) Growth rates and models. In: Hoar WS, Randall DJ, Brett JR (eds) Fish physiology, vol 8. Academic Press Inc, New York, pp 677–743

    Google Scholar 

  • Sahin K, Yazlak H, Orhan C, Tuzcu M, Akdemir F, Sahin N (2014) The effect of lycopene on antioxidant status in rainbow trout (Oncorhynchus mykiss) reared under high stocking density. Aquaculture 418:132–138

    Google Scholar 

  • Sahoo P, Kumari J, Mishra B (2005) Non-specific immune responses in juveniles of Indian major carps. J Appl Ichthyol 21:151–155

    Google Scholar 

  • Shakya SR (2017) Effect of herbs and herbal products feed supplements on growth in fishes: a review. Nepal J Biotechnol 5:58–63

    Google Scholar 

  • Siwicki AK, Anderson DP, Rumsey GL (1994) Dietary intake of immunostimulants by rainbow trout affects non-specific immunity and protection against furunculosis. Vet Immunol Immunop 41:125–139

    CAS  Google Scholar 

  • Sonmez AY, Bilen S, Alak G, Hisar O, Yanik T, Biswas G (2015a) Growth performance and antioxidant enzyme activities in rainbow trout (Oncorhynchus mykiss) juveniles fed diets supplemented with sage, mint and thyme oils. Fish Physiol Biochem 41:165–175

    CAS  PubMed  Google Scholar 

  • Sonmez AY, Bilen S, Albayrak M, Yilmaz S, Biswas G, Hisar O, Yanik T (2015b) Effects of dietary supplementation of herbal oils containing 1,8-cineole, carvacrol or pulegone on growth performance, survival, fatty acid composition, and liver and kidney histology of rainbow trout (Oncorhynchus mykiss) fingerlings. Turk J Fish Aquat Sc 15:813–819

    Google Scholar 

  • Taheri Mirghaed A, Hoseini SM, Ghelichpour M (2018) Effects of dietary 1,8-cineole supplementation on physiological, immunological and antioxidant responses to crowding stress in rainbow trout (Oncorhynchus mykiss) fish shellfish. Immunol 81:182–188

    CAS  Google Scholar 

  • Tang J, Cai J, Liu R, Wang J, Lu Y, Wu Z, Jian J (2014) Immunostimulatory effects of artificial feed supplemented with a Chinese herbal mixture on Oreochromis niloticus against Aeromonas hydrophila. Fish Shellfish Immunol 39:401–406

    CAS  PubMed  Google Scholar 

  • Vinothkumar V, Manoharan S, Sindhu G, Nirmal MR, Vetrichelvi V (2012) Geraniol modulates cell proliferation, apoptosis, inflammation, and angiogenesis during 7,12-dimethylbenz[a]anthracene-induced hamster buccal pouch carcinogenesis. Mol Cell Biochem 369:17–25

    CAS  PubMed  Google Scholar 

  • Worthington C (1988) Worthington enzyme manual: enzymes and related biochemicals. Worthington Biochemical Corporation

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Funding

This work was supported by the Kastamonu University, Scientific Research Project Coordinators with the project code of KÜBAP01/2016-41.

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Authors and Affiliations

  1. Faculty of Fisheries, Department of Aquaculture, Kastamonu University, Kastamonu, Turkey

    Soner Bilen, Keriman Yürüten Özdemir & Ertugrul Terzi

  2. Department of Basic Veterinary Medical Sciences, Omar Al-Mukhtar University, Al Bayda, Libya

    Tarek Abdalsalam Salem Altief

  3. Institute of Science, Department of Aquaculture, Kastamonu University, Kastamonu, Turkey

    Mohamed Omar Abdalla Salem

  4. Faculty of Forestry, Department of Forest Engineering, Kastamonu University, Kastamonu, Turkey

    Kerim Güney

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  1. Soner Bilen
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  2. Tarek Abdalsalam Salem Altief
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  5. Ertugrul Terzi
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Correspondence to Soner Bilen.

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All procedures were approved in advance by the local ethics committee for animal research studies at the Kastamonu University (KUHADYEK-09.05.2016–2016.17).

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Bilen, S., Altief, T.A.S., Özdemir, K.Y. et al. Effect of lemon balm (Melissa officinalis) extract on growth performance, digestive and antioxidant enzyme activities, and immune responses in rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 46, 471–481 (2020). https://doi.org/10.1007/s10695-019-00737-z

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