Shiitake Mantar Ekstraktı İlaveli Yemlerin Gökkuşağı Alabalığında (Oncorhynchus mykiss) Büyüme, Non-Spesifik İmmun Parametreler ve in-vitro Aeromonas hyrophila Enfeksiyonuna Karşı Direnç Üzerine Etkileri

Abstract

Bu çalışmada Lentinula edodes (shiitake) tıbbi mantar ekstraktının gökkuşağı alabalığının (Oncorhynchus mykiss) spesifik olmayan bağışıklık cevabı ve biyometrik performans üzerine etkileri incelenmiştir. Bu amaçla balıklar (başlangıç ağırlığı 20 g) iki tekrar olucak şekilde %1 ve %2 shiitake ekstraktı ilaveli yemlerle beslenen deneme grupları ve bir kontrol grubu olmak üzere üç gruba (60 balık/grup) ayrılmıştır. Deneme 45 gün sürmüştür. Beslenme sürecinde balıklardan 1., 2., 3., 4., 5. ve 6. haftalarda alınan kan ve serum örneklerinden immünolojik, biyokimyasal parametreler belirlenmiştir. Deneme başlangıcında ve sonunda balıklardan gerekli ölçümler yapılarak biyometrik analizler değerlendirilmiştir. İmmünolojik, biyokimyasal ve biyometrik parametrelerin sonuçlarına göre maksimum etkinin %2 shiitake ekstraktı ile beslenen gökkuşağı alabalığında meydana geldiğini belirlenmiştir. Deneme gruplarında balıkların kanında tespit edilen respiratory burst aktivitesi, kontrol grubuyla karşılaştırıldığında 2. ve 6. haftalarda artış gösterdiği tespit edilmiştir. Mantar ekstraktı ilaveli yemlerle beslenen balıklarda toplam protein miktarı, bakterisidal aktivitede önemli ölçüde artış göstermiştir. 3. ve 6. haftalarda %2 shiitake ekstraktı ilaveli yemlerle beslenen balıklarda kolesterol seviyesinin düştüğü belirlenmiştir. Elde edilen sonuçlara göre shiitake tıbbi mantar ekstraktı ilaveli yemlerle beslenen gökkuşağı alabalığının spesifik olmayan bağışıklık cevabının kontrol grubuna kıyasla ölçülen parametrelerde pozitif sonuçlar verdiği, aynı zamanda gökkuşağı alabalığının genel büyüme performansını arttığı belirlenmiştir.

Keywords

• gökkuşağı alabalığı
• shiitake
• ekstrakt
• stimulate
• non-spesifik sistem

Effects of Dietary Supplemented Shiitake Mushroom Extract on Growth, Non-specific Immune Parameters and in-vitro Resistance Against Aeromonas hydrophila in Rainbow Trout (Oncorhynchus mykiss)

Abstract

The activity of Lentinula edodes (shiitake) medicinal mushroom extract were examined on the non-specific immune response and biometrical performance of rainbow trout (Oncorhynchus mykiss). Fish (20 g initial weight) were divided into 3 treatment groups (60 fish/group) and duplicated groups for 6 weeks having two experimental diets supplemented with 1-2% shiitake extract and a control diet. During the feeding process, immunological, biochemical, and biometrical observations were determined using the fish and blood samples taken at weeks 1, 2, 3, 4, 5, and 6, respectively. The results of immunological, biochemical, and biometrical parameters evaluation determined that the maximum influence occurs in rainbow trout fed with 2% shiitake extract. The amount of respiratory burst activity in the blood of fish in the trial groups significantly increased in each diet on the 2nd and 6th weeks compared to controls. The amount of total protein, bactericidal activity were significantly increased in fish being fed a mushroom supplemented diet. Cholesterol level decreased in fish blood, which fed with 2% shiitake extract supplemented diet at 3rd and 6th weeks. These results support the findings that the non-specific immune responses of rainbow trout was stimulated in fish by feeding shiitake medicinal mushroom extract yielding positive results in measured parameters compared to the control group also enhancing the overall growth performance of rainbow trout.

Keywords

• rainbow trout
• shiitake
• extract
• stimulate,
• innate immunity

References

1. Anderson DP, Moritomo T, Grooth RD. 1992. Neutrophile, glass-adherent, nitroblue tetrazolium assay gives early indication of immunization effectiveness in rainbow trout. Vet Immunol Immunopathol. 30:419-429. doi: 10.1016/0165-2427(92)90110-c
2. AOAC. 2009. Official Methods of Analysis of AOAC International. 17th ed. Assoc. Official Analytical Chemists, Arlington, VA.
3. 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. doi: 10.1111/j.1365-2761.2009.01133.x
4. Awad E, Austin D, Lyndon AR. 2013. Effect of black cumin seed oil (Nigella sativa) and nettle extract (Quercetin) on enhancement of immunity in rainbow trout, Oncorhynchus mykiss (Walbaum). Aquaculture. 388-391:193-197. doi:10.1016/j.aquaculture.2013.01.008
5. Baba E, Uluköy G, Mammadov R. 2014. Effects of Muscari comosum extract on nonspecific immune parameters in gilthead seabream, Sparus aurata (L. 1758). J World Aquac Soc. 5(2):173-182. doi: 10.1016/j.fsi.2013.08.005
6. Basha KA, Raman RP, Prasad KP, Kumar K, Nilavan E, Kumar S. 2013. Effect of dietary supplemented andrographolide on growth, non-specific immune parameters and resistance against Aeromonas hydrophila in Labeo rohita (Hamilton). Fish Shellfish Immunol.35:1433-1441. doi: 10.1016/j.fsi.2013.08.005
7. Bernas E, Jaworska G, Lisiewska Z. 2006. Edible mushrooms as a source of valuable nutritive constituents. Acta Sci Pol Technol Aliment. 5(1): 5-20.
8. Bilen S, Bulut M, Bilen AM. 2011. Immunostimulant effects of Cotinus coggyria on rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol. 30:451-455. doi: https://doi.org/10.1016/j.fsi.2010.12.013

9. Binaii M, Ghiasi M, Farabi SV, Pourghola R, Fazli H, Safari R, Alavi SE, Taghavi MJ, Bankehsaz Z. 2014. Biochemical and hemato-immunological parameters in juvenile beluga (Huso huso) following the diet supplemented with nettle (Urtica dioica). Fish Shellfish Immunol. 36:46-51. doi: 10.1016/j.fsi.2013.10.001
10. Bobek P, Ozdin O, Mikus M. 1995. Dietary oyster mushroom (Pleurotus ostreatus) accelerates cholesterol turnover in hypercholesterolaemic rats. Phys Res. 44(5):287-291.
11. Bobek P, Ginter E, Kuniak L, Babala J, Jurcovicova M, Ozdin L, Cerven J. 1991. Effect of mushroom Pleurotus ostreatus and isolated fungal polysaccharide on serum and liver lipids in Syrian hamsters with hyperlipoproteinemia. Nutrition. 7:105-108.
12. Bradford MM. 1976. A rapid method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem. 72:248-254. doi: 10.1006/abio.1976.9999
13. Cabello FC. 2006. Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ Microbiol. 8:1137-1144. doi: 10.1111/j.1462-2920.2006.01054.x
14. Dalsgaard I, Madsen L. 2000. Bacterial pathogens in rainbow trout, Oncorhynchus mykiss (Walbaum), reared at danish freshwater farms. J Fish Dis. 23: 199-209. doi:https://doi.org/10.1046/j.1365-761.2000.00242.x
15. Dobšíková R, Blahová J, Fran A, Jakubík J, Mikulíková I, Modrá H, Novotná K, Svobodová Z. 2012. Effect of β-1.3/1.6-D-glucan derived from oyster mushroom Pleurotus ostreatus on biometrical, haematological, biochemical, and immunological indices in rainbow trout (Oncorhynchus mykiss). Neuro Endocrinol Lett. 33(3):101-111.
16. Dügenci SK, Arda N, Candan A. 2003. Some medicinal plants as immunostimulant for fish. J Ethnopharmacol.88:99-106. doi: 10.1016/s0378-8741(03)00182-x
17. Ellis AE. 2001. Innate host defence mechanism of fish against viruses and bacteria. Dev Comp Immunol. 25:827-839. doi: 10.1016/s0145-305x(01)00038-6
18. Elumalai P, Kurian A, Lakshmi S, faggio C, Esteban MA, Ringo E. 2021. Herbal Immunomodulators in Aquaculture. Rev. Fisheries Sci. Aquaculture. 29(1):33-57
19. Galindo-Villegas J, Hosokawa H. 2004. Immunostimulants: Towards temporary prevention of diseases in marine fish. Aquaculture. 16-19.
20. Guardiola FA, Bah A, Esteban A. 2018. Effects of dietary administration of fenugreek seeds on metabolic parameters and immune status of gilthead seabream (Sparus aurata L.). Fish Shellfish Immunol. 74:372-379. doi: 10.1016/j.fsi.2018.01.010
21. Guo FC, Williams BA, Kwakkel RP, Li HS, Li XP, Luo JY. 2004. Effects of mushroom and herb polysaccharides, as alternatives for an antibiotic, on the cecal microbial ecosystem in broiler chickens. Poult Sci. 83:175-182. doi: https://doi.org/10.1093/ps/83.2.175
22. Hwang JA, Hossain E, Yun DH, Moon ST, Kim M, Yang CJ. 2012. Effect of shiitake (Lentinula edodes (Berk.) Pegler) mushroom on laying performance, egg quality, fatty acid composition and cholesterol concentration of eggs in layer chickens. J Med Plants Res.6(1): 146-153. doi: 10.5897/JMPR11.1351
23. Harikrishnan R, Balasundaram C, Heo MS. 2012a. Effect of Inonotus obliquus enriched diet on hematology, immune response, and disease protection in kelp grouper, Epinephelus bruneus against Vibrio harveyi. Aquaculture. 344-349:48-53. doi:https://doi.org/10.1016/j.aquaculture.2012.03.010
24. Harikrishnan R, Balasundaram C, Heo MS. 2012b. Inonotus obliquus containing diet enhances the innate immune mechanism and disease resistance in olive flounder (Paralichythys olivaceus) against Uronema marinum. Fish Shellfish Immunol. 32(6):1148-1154. doi: 10.1016/j.fsi.2012.03.021.
25. Hoseinifar, SH, Sun YZ, Zhou Z, Doan HV, Davies SJ, Harikrishnan R. 2020. Boosting Immune Function and Disease Bio-Control Through Environment-Friendly and Sustainable Approaches in Finfish Aquaculture: Herbal Therapy Scenarios. Rev. Fisheries Sci. Aqua. 28(3):303-321. doi:10.1080/23308249.2020.1731420
26. Kajita Y, Sakai M, Atsuda S, Kobayashi M. 1990. The immunonodulatory effect of levamisole on rainbow trout Oncorhynchus mykiss. Fish Pathol. 25:93-98.
27. Kanani HG, Nobahar Z, Kakoolaki S, Jafarian H. 2014. Effect of ginger and garlic supplemented diet on growth performance, some hematological parameters and immune responses in juvenile Huso huso. Fish Physiol Biochem. 40:481-490. doi: 10.1007/s10695-013-9859-6
28. Kumar S, Raman P, Pandey PK, Mohanty S, Kumar A, Kumar K. 2013. Effect of orally administered azadirachtin on non-specific immune parameters of goldfish Carassius auratus (Linn. 1758) and resistance against Aeromonas hydrophila. Fish Shellfish Immunol. 34:564-573. doi: 10.1016/j.fsi.2012.11.038
29. Kwak JK, Park SW, Koo JG, Cho MG, Buchholz R, Goetz P. 2003. Enhancement of the non-specific defence activities in carp (Cyprinus carpio) and flounder (Paralichthys olivcaces) by oral administration of schizophyllan. Acta Biotechnol. 23(4): 359-371. doi: https://doi.org/10.1002/abio.200390046
30. Laird L, Needham T. 1988. Salmon and trout farming, Harwood, New York.
31. Laith AA, Mazla AG, Effendy AW, Ambak MA, Nurhafizah WWI, Ali A, Jabar A, Najiah M. 2017. Effect of Excoecaria agallocha on non-specific immune responses and disease resistance of Oreochromis niloticus against Streptococcus agalactiae. Res Vet Sci. 112: 192-200. doi: 10.1016/j.rvsc.2017.04.020
32. Li P, Gatlin DM. 2005. Evaluation of the prebiotic GroBiotic AE and brewer’s yeast as dietary supplements for sub-adult hybrid striped bass (Morone chrysopsx x M. saxatilis) challenged in situ with (Mycobacterium marinum). Aquaculture. 248:197-205. doi: 10.1016/j.aquaculture.2005.03.005
33. Logambal SM, Venkatalakshmi S, Dinakaran MR. 2000. Immunostimulatory effect of Ocimum sanctum Linn. in Oreochromis mossambicus (Peters). Hydrobiologia. 430:113-120.
34. Magnadottir B. 2006. Innate immunity of fish. Fish Shellfish Immunol. 20:137-151. doi: https://doi.org/10.1016/j.fsi.2004.09.006
35. Mau J, Lin H, Song S. 2002. Antioxidant properties of several specialty mushrooms. Food Res Int. 3: 519-526. doi: https://doi.org/10.1016/S0963-9969(01)00150-8
36. Mizuno T. 1995. Shiitake, Lentinus edodes: functional properties for medicinal and food purposes. Food Rev Int.11:7-21. doi: https://doi.org/10.1080/87559129509541022
37. Nya E, Austin B. 2009a. Use of dietary ginger, Zingiber officinale Roscoe, as an immunostimulant to control Aeromonas hydrophila infections in rainbow trout, (Oncorhynchus mykiss). J Fish Dis. 32:971-977. doi: 10.1111/j.1365-2761.2009.01101.x
38. Nya E, Austin B. 2009b. Use of garlic, Allium sativum, to control Aeromonas hydrophila infection in rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis. 32:963-970. doi: 10.1111/j.1365-2761.2009.01100.x
39. Nya EJ, Austin B. 2011. Development of immunity in rainbow trout (Oncorhynchus mykiss, Walbaum) to Aeromonas hydrophila after the dietary application of garlic. Fish Shellfish Immunol. 30:845-850. doi: 10.1016/j.fsi.2011.01.008
40. Rao YV, Chakrabarti R. 2005. Stimulation of immunity in Indian major carp Catla catla with herbal feed ingredients. Fish Shellfish Immunol. 18(4):327–334. https://doi.org/10.1016/j.fsi.2004.08.005
41. Reguła J, Siwulski M. 2007. Dried shiitake (Lentınulla edodes) and oyster (Pleurotus ostreatus) mushrooms as a good source of nutrient. Acta Sci Pol Technol Aliment. 6(4):135-142.
42. Sheikhzadeh N, Nofouzi K, Delazar A, Oushani AK. 2011. Immunomodulatory effects of decaffeinated green tea (Camellia sinensis) on the immune system of rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol. 31:1268-1269. doi: 10.1016/j.fsi.2011.09.010
43. Sheikhzadeh N, Heidarieh M, Pashaki K, Nofouzi K, Farshbafii MA, Akbar M. 2012. Hilyses, fermented Saccharomyces cerevisiae, enhances the growth performance and skin non-specific immune parameters in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol. 32:1083-1087. doi: 10.1016/j.fsi.2012.03.003
44. Sivaram V, Babu MM, Immanul G, Murugadass S, Citarasu T, Petermarian M. 2004. Growth and immunoresponse of juvenile greasy groupers (Epinephelus tauvina) fed with herbal antibacterial active principle supplemented diets against Vibrio harveyi infection. Aquaculture.237:9-20. doi:https://doi.org/10.1016/j.aquaculture.2004.03.014
45. Smith J, Rowan N, Sullivan R. 2002. Medicinal mushrooms: Their therapeutic properties and current medical usage with special emphasis on cancer treatments. Univ. Strathclyde, Glasgow, UK.
46. Stratev D, Zhelyazkov G, Noundou XN, Krause RM. 2018. Beneficial effects of medicinal plants in fish diseases. Aquacult Int. 26:289-308. doi: 10.1007/s10499-017-0219-x
47. Talpur AD, Ikhwanuddi M. 2013. Azadirachta indica (neem) leaf dietary effects on the immunity response and disease resistance of Asian seabass, Lates calcarifer challenged with Vibrio harveyi. Fish Shellfish Immunol. 34:254-264. doi: 10.1016/j.fsi.2012.11.003
48. 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. doi: 10.1016/j.fsi.2014.05.028
49. Van Hai N. 2015. The use of medicinal plants as immunostimulants in aquaculture: a review. Aquaculture.446:88–96. doi:10.1016/j.aquaculture.2015.03.014
50. Wang JL, Meng X, Lu R, Wu C, Luo YT, Yan X, Li XJ, Kong XH, Nie GX. 2015. Effects of Rehmannia glutinosa on growth performance, immunological parameters and disease resistance to Aeromonas hydrophila in common carp (Cyprinus carpio L.). Aquaculture.435:293-300. doi:https://doi.org/10.1016/j.aquaculture.2014.10.004
51. Wiegertjes GF, Stet RJM, Parmentier HK, Van Muiswinkel WB. 1996. Immunogenetics of disease resistance in fish; a comparable approach. Dev Comp Immunol.20:365-381. doi: 10.1016/s0145-305x(96)00032-8
52. Xu C, Yan ZH, Hong ZJ, Jing G. 2008. The pharmacological effect of polysaccharides from Lentinus edodes on the oxidative status and expression of VCAM-1mRNA of thoracic aorta endothelial cell in high-fat-diet rats. Carbohydr Polym.74:445-450. https://doi.org/10.1016/j.carbpol.2008.03.018
53. Yang H, Hwang I, Kim S, Hong EJ, Jeung EB. 2013. Lentinus edodes promotes fat removal in hyper cholesterolomic mice. Exp Ther Med. 6(6): 1409-1413. doi: 10.3892/etm.2013.1333
54. Yap AT, Ng MLM. 2001. An improved method for the isolation of lentinan from the edible and medicinal shiitake mushroom, Lentinus edodes (Berk.) Sing. (Agaricomycetideae). Int J Med Mushrooms. 3:6-19.
55. Yin G, Ardo L, Jeney Z, Xu P, Jeney G. 2008. In Bondad-Reantaso MG, Mohan CV, Crumlish M, Subasinghe RP. Editors. Chinese herbs (Lonicera japonica and Ganoderma lucidum) enhance non-specific immune response of tilapia, Oreochromis niloticus, and protection against Aeromonas hydrophila. Diseases in Asian Aquaculture VI. Fish Health Section, Asian Fisheries Society, Manila, Philippines 269-282 p.
56. Zahran E, Risha E, AbdelHamid F, Mahgou HA, Ibrahim T. 2014. Effects of dietary Astragalus polysaccharides (APS) on growth performance, immunological parameters, digestive enzymes, and intestinal morphology of Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol. 38:149-157. doi:10.1016/j.fsi.2014.03.002