Skip to main content
SpringerLink
Log in

Immunostimulating effects of Ginkgo biloba extract against toxicity induced by organophosphate pesticide, diazinon in rainbow trout, Oncorhynchus mykiss: innate immunity components and immune-related genes

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The immunostimulating and therapeutic properties of Ginkgo biloba (GB) have always been the focus of traditional medicine over thousands of years. During last decade, special attentions were paid to use of GB in aquaculture to enhance fish health and survival. In the present study, we investigated for the first time the immunogenic effects of dietary GB against oxidative and toxicity induced by organophosphate pesticide, diazinon. In non-diazinon-exposed fish, the plasma total immunoglobulin, lysozyme activity, and peroxidase activity significantly elevated after 60-day experiment in fish supplemented with 1 and 2 g GB/kg diet (p < 0.05). The respiratory burst activity and complement activity significantly increased only in groups supplemented with 0.5 g GB/kg diet (p < 0.05). Furthermore, the peroxidase activity, total immunoglobulin, and lysozyme activity significantly declined in groups supplemented with 4 g GB/kg diet during feeding trial (p < 0.05). There were no significant differences in expression of interleukin 1 beta (IL-1β) and transforming growth factor beta 1 (TGF-β1) genes in kidney between control group (non-GB-supplemented fish) and GB-supplemented fish (p > 0.05). In diazinon-exposed fish, all immunity components significantly decreased during exposure in control and those fed 0.5 and 4 g GB/kg diet (p < 0.05). In fish fed 1 and 2 g GB/kg diet, no alternations were found in immunity components during exposure period (p > 0.05). In addition, diazinon induced the expression of IL-1β and TGF-β1 genes in control and fish fed 0.5 and 4 g GB/kg diet (p < 0.05). No significant changes were observed in expression of IL-1β and TGF-β1 genes in fish supplemented with 1 and 2 g GB/kg (p > 0.05). In conclusion, the results of the present study suggest an immunogenic role for dietary GB at optimum dietary levels (1–2 g GB/kg diet) against toxicity induced by diazinon. Nevertheless, GB at high dietary levels (4 g GB/kg diet) showed immunosuppressive effects, which makes it necessary to optimize its levels in diet.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ahmadi K, Mirvaghefei AR, Banaee M, Vosoghei AR (2014) Effects of long-term diazinon exposure on some immunological and haematological parameters in rainbow trout Oncorhynchus mykiss (Walbaum, 1792). Toxicol Environ Heal Sci 6(1):1–7

    Article  Google Scholar 

  • Andreson DP, Zeeman MG (1995) Immunotoxicology in fish. In: Rand GM (ed) Fundamentals of aquatic toxicology. Taylorand Francis, Washington, pp 371–404

    Google Scholar 

  • Arufe MI, Arellano JM, García L, Albendín G, Sarasquete C (2007) Cholinesterase activity in gilthead seabream (Sparus aurata) larvae: characterization and sensitivity to the organophosphate azinphosmethyl. Aquat Toxicol 84(3):328–336

    Article  CAS  Google Scholar 

  • Awad E, Mitchell WJ, Austin B (2011) Effect of dietary supplements on cytokine gene expression in rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 34(8):629–634

    Article  CAS  Google Scholar 

  • Banaee M, Mirvagefei AR, Rafei GR, Majazi Amiri B (2008) Effect of sub-lethal diazinon concentrations on blood plasma biochemistry. Int J Environ Res 2(2):189–198

    CAS  Google Scholar 

  • Banaee M, Sureda A, Mirvaghefi AR, Ahmadi K (2011) Effects of diazinon on biochemical parameters of blood in rainbow trout (Oncorhynchus mykiss). Pestic Biochem Physiol 99(1):1–6

    Article  CAS  Google Scholar 

  • Banaee M, Sureda A, Shahaf S, Fazilat N (2015) Protective effects of silymarin extract on malthion-induced zebra cichlid (Cichlasomanigrofasciatum) hepatotoxicity. Iran J Toxicol 9(28):1239–1246

    CAS  Google Scholar 

  • Bridi R, Crossetti FP, Steffen VM, Henriques AT (2001) The antioxidant activity of standardized extract of Ginkgo biloba (EGb 761) in rats. Phytother Res 15(5):449–451

    Article  CAS  Google Scholar 

  • Cao F, Lu Y, Zhang X, Zhao L, Yang J, Qin X, Yu W (2015) Effects of dietary supplementation with fermented Ginkgo leaves on innate immunity, antioxidant capability, lipid metabolism, and disease resistance against Aeromonas hydrophila infection in blunt snout bream (Megalobrama amblycephala). Isr J Aquac 67:1202–1212

  • Çavușoğlu K, Yapar K, Yalcin E (2009) Antioxidant potential of Ginkgo biloba leaf extract against uranium-induced genotoxicity and oxidative stress in albino mice. Fresenius Environ Bull 18(9):1551–1558

    Google Scholar 

  • Çavuşoğlu K, Yapar K, Oruç E, Yalçın E (2011) Protective effect of Ginkgo biloba L. leaf extract against glyphosate toxicity in Swiss albino mice. J Med Food 14(10):1263–1272

    Article  CAS  Google Scholar 

  • Chakraborty SB, Hancz C (2011) Application of phytochemicals as immunostimulant, antipathogenic and antistress agents in finfish culture. Rev Aquac 3(3):103–119

    Article  Google Scholar 

  • Chan PC, Xia Q, Fu PP (2007) Ginkgo biloba leave extract: biological, medicinal, and toxicological effects. J Environ Sci Health Part C 25(3):211–244

    Article  CAS  Google Scholar 

  • Chávez-Morales RM, Jaramillo-Juárez F, Posadas del Río FA, Reyes-Romero MA, Rodríguez-Vázquez ML, Martínez-Saldaña MC (2011) Protective effect of Ginkgo biloba extract on liver damage by a single dose of CCl 4 in male rats. Hum Exp Toxicol 30(3):209–216

    Article  CAS  Google Scholar 

  • Citarasu T, Jayarani TV, Babu MM, Marian MP (1999) Use of herbal bio-medicinal products in aquaculture of shrimp. In Aqua-Terr Annual Symposium, School of Biological Sciences, MK University, Madurai (p. 83)

  • Citarasu T, Babu MM, Punitha SMJ, Ramalingam V, Marian MP (2001) Control of pathogenic bacteria using herbal biomedical products in the larviculture system of Peneaus monodon. In: Int. Con. Ad. Tech. Fish Mar. Sci. Indian Council of Agricultural Science, M.S. University, Nagercoil, India

  • Citarasu T, VenketRamalingam K, Raja JeyaSekar R, MichealBabu M, Marian MP (2002) Influence of the antibacterial herbs, Solanum trilobatum, Andrographis paniculata and Psoraleacorylifolia on the survival, growth and bacterial load of Penaeus monodon post larvae. Aquac Int 11:583–595

    Google Scholar 

  • Cooper CM (1993) Biological effects of agriculturally derived surface water pollutants on aquatic systems—a review. J Environ Qual 22(3):402–408

    Article  CAS  Google Scholar 

  • Demers NE, Bayne CJ (1997) The immediate effects of stress on hormones and plasma lysozyme in rainbow trout. Dev Comp Immunol 21(4):363–373

    Article  CAS  Google Scholar 

  • Dunier M, Siwicki AK (1993) Effects of pesticides and other organic pollutants in the aquatic environment on immunity of fish: a review. Fish Shellfish Immunol 3(6):423–438

    Article  Google Scholar 

  • Eder KJ, Leutenegger CM, Wilson BW, Werner I (2004) Molecular and cellular biomarker responses to pesticide exposure in juvenile Chinook salmon (Oncorhynchus tshawytscha). Mar Environ Res 58(2–5):809–813

    Article  CAS  Google Scholar 

  • Eder KJ, Clifford MA, Hedrick RP, Köhler HR, Werner I (2008) Expression of immune-regulatory genes in juvenile Chinook salmon following exposure to pesticides and infectious hematopoietic necrosis virus (IHNV). Fish Shellfish Immunol 25(5):508–516

    Article  CAS  Google Scholar 

  • El-Gendy KS, Aly NM, El-Sebae AH (1998) Effects of edifenphos and glyphosate on the immune response and protein biosynthesis of bolti fish (Tilapia nilotica). J Environ Sci Health Part B 33(2):135–149

    Article  CAS  Google Scholar 

  • Fatima M, Mandiki SNM, Douxfils J, Silvestre F, Coppe P, Kestemont P (2007) Combined effects of herbicides on biomarkers reflecting immune–endocrine interactions in goldfish: immune and antioxidant effects. Aquat Toxicol 81(2):159–167

    Article  CAS  Google Scholar 

  • Galina J, Yin G, Ardo L, Jeney Z (2009) The use of immunostimulating herbs in fish. An overview of research. Fish Physiol Biochem 35(4):669–676

    Article  CAS  Google Scholar 

  • Galloway T, Handy R (2003) Immunotoxicity of organophosphorous pesticides. Ecotoxicol 12(1–4):345–363

    Article  CAS  Google Scholar 

  • Girón-Pérez MI, Santerre A, Gonzalez-Jaime F, Casas-Solis J, Hernández-Coronado M, Peregrina-Sandoval J, Takemura A, Zaitseva G (2007) Immunotoxicity and hepatic function evaluation in Nile tilapia (Oreochromis niloticus) exposed to diazinon. Fish Shellfish Immunol 23(4):760–769

    Article  CAS  Google Scholar 

  • Guilherme S, Gaivão I, Santos MA, Pacheco M (2012) DNA damage in fish (Anguilla anguilla) exposed to a glyphosate-based herbicide–elucidation of organ-specificity and the role of oxidative stress. Mutat Res Genet Toxicol Environ Mutagen 743(1):1–9

    Article  CAS  Google Scholar 

  • Kampkötter A, Pielarski T, Rohrig R, Timpel C, Chovolou Y, Wätjen W, Kahl R (2007) The Ginkgo biloba extract EGb761 reduces stress sensitivity, ROS accumulation and expression of catalase and glutathione S-transferase 4 in Caenorhabditiselegans. Pharmacol Res 55(2):139–147

    Article  CAS  Google Scholar 

  • Khoshbavar-Rostami HA, Soltani M, Hassan HMD (2006) Immune response of great sturgeon (Huso huso) subjected to long-term exposure to sublethal concentration of the organophosphate, diazinon. Aquac 256(1–4):88–94

    Article  CAS  Google Scholar 

  • Kleijnen J, Knipschild P (1992) Ginkgo biloba. Lancet 340(8828):1136–1139

    Article  CAS  Google Scholar 

  • Kreutz LC, Barcellos LJG, de Faria VS, de Oliveira ST, Anziliero D, dos Santos ED, Pivato M, Zanatta R (2011) Altered hematological and immunological parameters in silver catfish (Rhamdia quelen) following short term exposure to sublethal concentration of glyphosate. Fish Shellfish Immunol 30(1):51–57

    Article  CAS  Google Scholar 

  • Krithika R, Verma RJ (2014) Ameliorative effects of phyllanthin on carbon tetrachloride-induced hepatic oxidative damage in mice. Asian Pac J Trop Dis 4:S64–S70

    Article  CAS  Google Scholar 

  • Lackner R (1998) “Oxidative stress” in fish by environmental pollutants. In: Fish ecotoxicology. Birkhäuser, Basel, pp 203–224

  • Li X, Liu L, Zhang Y, Fang Q, Li Y, Li Y (2013) Toxic effects of chlorpyrifos on lysozyme activities, the contents of complement C3 and IgM, and IgM and complement C3 expressions in common carp (Cyprinus carpio L.). Chemosphere 93(2):428–433

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25(4):402–408

    Article  CAS  Google Scholar 

  • Loganathan BG, Kannan K (1991) Time perspectives of organochlorine contamination in the global. Mar Pollut Bull 22(12):582–584

    Article  CAS  Google Scholar 

  • Loganathan BG, Kannan K (1994) Global organochlorine contamination trends: an overview. Ambio 23:187–191

  • Ma J, Feng Y, Xie W, Yang L, Li X (2015) Immune response in common carp (Cyprinus carpio L.) following glyphosate-exposure. Toxin Rev 34(4):184–189

    Article  CAS  Google Scholar 

  • Marcocci L, Maguire JJ, Droylefaix MT, Packer L (1994a) The nitric oxide-scavenging properties of Ginkgo biloba extract EGb 761. Biochem Biophys Res Commun 201(2):748–755

    Article  CAS  Google Scholar 

  • Marcocci L, Packer L, Droy-Lefaix MT, Sekaki A, Gardès-Albert M (1994b) [46] antioxidant action of Ginkgo biloba extract EGb 761. In Methods in enzymology (Vol. 234, pp. 462-475). Academic Press

  • Miandare HK, Farahmand H, Akbarzadeh A, Ramezanpour S, Kaiya H, Miyazato M, Rytkönen KT, Nikinmaa M (2013) Developmental transcription of genes putatively associated with growth in two sturgeon species of different growth rate. Gen Comp Endocrinol 182:41–47

    Article  CAS  Google Scholar 

  • Mondon JA, Duda S, Nowak BF (2000) Immune response of greenback flounder Rhombosoleatapirina after exposure to contaminated marine sediment and diet. Mar Environ Res 50(1–5):443–450

    Article  CAS  Google Scholar 

  • Mora S, Diaz-Veliz G, Lungenstrass H, Garcia-Gonzalez M, Coto-Morales T, Poletti C, De Lima TCM, Herrera-Ruiz M, Tortoriello J (2005) Central nervous system activity of the hydroalcoholic extract of Casimiroaedulis in rats and mice. J Ethnopharmacol 97(2):191–197

    Article  CAS  Google Scholar 

  • Nayak AS, Lage CR, Kim CH (2007) Effects of low concentrations of arsenic on the innate immune system of the zebrafish (Danio rerio). Toxicol Sci 98(1):118–124

    Article  CAS  Google Scholar 

  • Nowell LH, Capel PD, Dileanis PD (1999) Pesticides in stream sediment and aquatic biota: distribution, trends, and governing factors. CRC Press, Boca Raton

    Book  Google Scholar 

  • Nya EJ, Austin B (2009) Use of dietary ginger, Zingiber officinale roscoe, as an immunostimulant to control Aeromonas hydrophila infections in rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 32(11):971–977

    Article  CAS  Google Scholar 

  • Ortuno J, Esteban MA, Meseguer J (2001) Effects of short-term crowding stress on the gilthead seabream (Sparusaurata L.) innate immune response. Fish Shellfish Immunol 11(2):187–197

    Article  CAS  Google Scholar 

  • Parvez S, Raisuddin S (2005) Protein carbonyls: novel biomarkers of exposure to oxidative stress-inducing pesticides in freshwater fish Channapunctata (Bloch). Environ Toxicol Pharmacol 20(1):112–117

    Article  CAS  Google Scholar 

  • Prasad S, Variyur Padhyoy KB (1993) Chemical investigation of some commonly used spices. Aryavaidyan 6(4):262–267

    Google Scholar 

  • Puebla-Pérez AM, Lozoya X, Villaseñor-García MM (2003) Effect of Ginkgo biloba extract, EGb 761, on the cellular immune response in a hypothalamic–pituitary–adrenal axis activation model in the rat. Int Immunopharmacol 3(1):75–80

    Article  Google Scholar 

  • Qichun H, Xintian Z, Xiaoyan Y (2012) The modulatory role of Ginkgo biloba extract on improving the immune function of weaned piglets. J Northwest Agri For Univ 11:23–28

  • Quade MJ, Roth JA (1997) A rapid, direct assay to measure degranulation of bovine neutrophil primary granules. Vet Immunol Immunopathol 58(3–4):239–248

    Article  CAS  Google Scholar 

  • Rabie M, Asri Y, Ahmadi K (2016) Effect of Milk thistle plant, Vitis vinifera extract on immune system of rainbow trout (Oncorhynchus mykiss) challenge by diazinon. Int J Aqua Biol 4(3):208

    Google Scholar 

  • Raj S, Gothandam KM (2014) Hepatoprotective effect of polyphenols rich methanolic extract of Amorphophalluscommutatus var. wayanadensis against CCl4 induced hepatic injury in swiss albino mice. Food Chem Toxicol 67:105–112

    Article  CAS  Google Scholar 

  • Raymond M (1985) Log-probit analysis program presentation for a microcomputer. Entomologie Médicale et Parasitologie 23(2):117–121

  • Reverter M, Bontemps N, Lecchini D, Banaigs B, Sasal P (2014) Use of plant extracts in fish aquaculture as an alternative to chemotherapy: current status and future perspectives. Aquac 433:50–61

    Article  Google Scholar 

  • Secombes CJ, Bird S, Cunningham C, Zou J (1999) Interleukin-1 in fish. Fish Shellfish Immunol 9(4):335–343

    Article  Google Scholar 

  • Shaaban AA, Shaker ME, Zalata KR, El-Kashef HA, Ibrahim TM (2014) Modulation of carbon tetrachloride-induced hepatic oxidative stress, injury and fibrosis by olmesartan and omega-3. Chem Biol Interact 207:81–91

    Article  CAS  Google Scholar 

  • Shelley LK, Balfry SK, Ross PS, Kennedy CJ (2009) Immunotoxicological effects of a sub-chronic exposure to selected current-use pesticides in rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 92(2):95–103

    Article  CAS  Google Scholar 

  • Sivaram JJ, Wu Z (2004) Effect of Chinese herbal medicine on non-specific immunity of Jian common carp (Cyprinuscarpio var. Jian). J Dalian Fish Univ 17:114–119

    Google Scholar 

  • Siwicki AK, Anderson DP (1993) Nonspecific defense mechanisms assay in fish: II. Potential killing activity of neutrophils and macrophages, lysozyme activity in serum and organs and total immunoglobulin level in serum. Fish Disease Diagnosis and Prevention Methods, FAO-Project GCP/INT/526/JPN, IFI Olsztyn, pp 105–112

  • Siwicki AK, Terech-Majewska E, Grudniewska J, Malaczewska J, Kazun K, Lepa A (2010) Influence of deltamethrin on nonspecific cellular and humoral defense mechanisms in rainbow trout (Oncorhynchus mykiss). Environ Toxicol Chem 29(3):489–491

    Article  CAS  Google Scholar 

  • Slaninova A, Smutna M, Modra H, Svobodova Z (2009) REVIEWS oxidative stress in fish induced by pesticides. Neuro Endocrinol Lett 30(1):2

    CAS  Google Scholar 

  • Sun H (2009) The effects of Ginkgo biloba leaf extract (GBE) on cytochrome P4503A and lysozyme activity in crucian carp (Carassius auratus). Fish Sci (Dalian) 28(12):760–762

    CAS  Google Scholar 

  • Tan X, Sun Z, Liu Q, Ye H, Zou C, Ye C, Lin H (2018) Effects of dietary ginkgo biloba leaf extract on growth performance, plasma biochemical parameters, fish composition, immune responses, liver histology, and immune and apoptosis-related genes expression of hybrid grouper (Epinephelus lanceolatus♂× Epinephelus fuscoguttatus♀) fed high lipid diets. Fish Shellfish Immunol 72:399–409

  • Tao R, Wang CZ, Ye JZ, Zhou H, Chen HX, Zhang YS (2014) Antibacterial/antifungal activity and synergistic interactions between C70–C120 polyprenol homologs from Ginkgo biloba L. leaves and the corresponding synthetic derivatives. Eur Food Res Technol 239(4):587–594

    Article  CAS  Google Scholar 

  • Tellez-Bañuelos MC, Santerre A, Casas-Solis J, Bravo-Cuellar A, Zaitseva G (2009) Oxidative stress in macrophages from spleen of Nile tilapia (Oreochromis niloticus) exposed to sublethal concentration of endosulfan. Fish Shellfish Immunol 27(2):105–111

    Article  CAS  Google Scholar 

  • Tian YM, Tian HJ, Zhang GY, Dai YR (2003) Effects of Ginkgo biloba extract (EGb 761) on hydroxyl radical-induced thymocyte apoptosis and on age-related thymic atrophy and peripheral immune dysfunctions in mice. Mech Ageing Dev 124(8–9):977–983

    Article  Google Scholar 

  • Tsuda T, Kojima M, Harada H, Nakajima A, Aoki S (1997) Acute toxicity, accumulation and excretion of organophosphorous insecticides and their oxidation products in killifish. Chemosphere 35(5):939–949

    Article  CAS  Google Scholar 

  • Tukmechi A, Rezaee J, Nejati V, Sheikhzadeh N (2014) Effect of acute and chronic toxicity of paraquat on immune system and growth performance in rainbow trout, Oncorhynchus mykiss. Aquac Res 45(11):1737–1743

    CAS  Google Scholar 

  • Valavanidis A, Vlahogianni T, Dassenakis M, Scoullos M (2006) Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol Environ Saf 64(2):178–189

    Article  CAS  Google Scholar 

  • Van Hai N (2015) The use of medicinal plants as immunostimulants in aquaculture: a review. Aquac 446:88–96

    Article  CAS  Google Scholar 

  • Velisek J, Svobodova Z, Machova J (2009) Effects of bifenthrin on some haematological, biochemical and histopathological parameters of common carp (Cyprinus carpio L.). Fish Physiol Biochem 35(4):583–590

    Article  CAS  Google Scholar 

  • Villaseñor-García MM, Lozoya X, Osuna-Torres L, Viveros-Paredes JM, Sandoval-Ramírez L, Puebla-Pérez AM (2004) Effect of Ginkgo biloba extract EGb 761 on the nonspecific and humoral immune responses in a hypothalamic–pituitary–adrenal axis activation model. Int Immunopharmacol 4(9):1217–1222

    Article  CAS  Google Scholar 

  • Wang D, Zhao Y, Sun Y, Yang X (2014) Protective effects of Ziyang tea polysaccharides on CCl4-induced oxidative liver damage in mice. Food Chem 143:371–378

    Article  CAS  Google Scholar 

  • Weeks BA, Warinner JE (1984) Effects of toxic chemicals on macrophage phagocytosis in two estuarine fishes. Mar Environ Res 14(1–4):327–335

    Article  CAS  Google Scholar 

  • Yang XY, Lin YX, Li Y (2008) Effect of ginkgo biloba extract on growth performance, slaughter performance and immune index in broilers [J]. J Fujian Agri For Univ (Natural Science Edition) 3:016

    Google Scholar 

  • Yonar SM (2013) Toxic effects of malathion in carp, Cyprinuscarpiocarpio: protective role of lycopene. Ecotoxicol Environ Saf 97:223–229

    Article  CAS  Google Scholar 

  • Zahran E, Risha E, Awadin W, Palić D (2018) Acute exposure to chlorpyrifos induces reversible changes in health parameters of Nile tilapia (Oreochromis niloticus). Aquat Toxicol 197:47–59

    Article  CAS  Google Scholar 

  • Zhang Z, Chen S, Mei H, Xuan J, Guo X, Couch L, Dobrovolsky VN, Guo L, Mei N (2015) Ginkgo biloba leaf extract induces DNA damage by inhibiting topoisomerase II activity in human hepatic cells. Sci Rep 5:14633

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors express their sincere gratitude to the people who lent their time, advice, and support to this study.

Funding

This study was supported by university of Jiroft under the grant No. 4813-97-7.

Author information

Authors and Affiliations

  1. Department of Fisheries and Environmental Sciences, Faculty of Natural Resources, University of Jiroft, Jiroft, Kerman, Iran

    Saeed Hajirezaee & Ahmad Rafieepour

  2. Department of food hygiene and quality control, Faculty of veterinary medicine, Shahrekord University, Shahrekord, Iran

    Shafigh Shafiei

  3. Department of Fisheries and Environmental Sciences, Faculty of Natural Resources and Earth Sciences, Shahrekord University, Shahrekord, Iran

    Ruhollah Rahimi

Authors
  1. Saeed Hajirezaee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ahmad Rafieepour
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shafigh Shafiei
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ruhollah Rahimi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Saeed Hajirezaee.

Additional information

Responsible editor: Philippe Garrigues

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hajirezaee, S., Rafieepour, A., Shafiei, S. et al. Immunostimulating effects of Ginkgo biloba extract against toxicity induced by organophosphate pesticide, diazinon in rainbow trout, Oncorhynchus mykiss: innate immunity components and immune-related genes. Environ Sci Pollut Res 26, 8798–8807 (2019). https://doi.org/10.1007/s11356-019-04327-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-04327-7

Keywords

Search

Navigation