Skip to main content
SpringerLink
Log in

Modulatory role of dietary Thymus vulgaris essential oil and Bacillus subtilis against thiamethoxam-induced hepatorenal damage, oxidative stress, and immunotoxicity in African catfish (Clarias garipenus)

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

Abstract

Thiamethoxam (TMX) is a widely used neonicotinoid insecticide for its effective potential for controlling insects from the agricultural field, which might induce toxicity to the aquatic biota. In this study, the role of the probiotic Bacillus subtilis (BS) and a phytogenic oil extract of Thymus vulgaris essential oil (TVEO) in the modulation of thiamethoxam (TMX)-induced hepatorenal damage, oxidative stress, and immunotoxicity in African catfish (Clarias garipenus) has been evaluated. Fish were subjected to TMX (5 mg L−1) and fed with a diet either supplemented with BS (1000 ppm) or TVEO (500 ppm). The experiment lasted for 1 month. By the end of the experiment, blood was sampled for biochemical analysis and fish organs and tissues were collected for histopathological and immunohistochemical examinations. Results showed a substantial increase of serum markers of hepatorenal damage such as the activities of aspartate transaminase (AST), alanine transaminase (ALT), and alkaline phosphatase (ALP) and levels of blood urea nitrogen (BUN) and creatinine with an obvious decrease of serum protein levels in the TMX-intoxicated group. Also, there was a considerable increase in malondialdehyde (MDA) levels and glutathione-S-transferase (GST) activity. TMX remarkably suppressed serum lysozyme activity, respiratory burst activity, and phagocytosis with a conspicuous elevation of the levels of interleukins (interleukin-1 beta (IL-1β) and interleukin-6 IL-6). The histopathological findings showed that TMX induced degenerative changes and necrosis in the gills, liver, head kidneys, and spleen of the intoxicated fish. Significant alterations of frequency, size, and area percentage of melanomacrophage centers (MMCs), decreased splenocyte proliferation, and increased number of caspase-3 immunopositive cells were also observed. Contrariwise, the concurrent supplementation of either BS or TVEO in the diets of catfish partially mitigated both the histopathological and histomorphometric lesions of the examined tissues. Correspondingly, they improved the counts of proliferating cell nuclear antigen (PCNA) and caspase-3 immunopositive splenocytes. In conclusion, the co-administration of either BS or TVEO in catfish diets partially diminished the toxic impacts of TMX. Nonetheless, the inclusion of TVEO in the diets of catfish elicited better protection than BS against TMX-induced toxicity in response to its potential anti-inflammatory, antioxidant, anti-apoptotic, and immune-stimulant effects.

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
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abalaka SE (2013) Evaluation of the haematology and biochemistry of Clarias gariepinus as biomakers of environmental pollution in Tiga dam, Nigeria. Braz Arch Biol Technol 56(3):371–376

  • Abdel-Azeem AS, Hegazy AM, Zeidan HM, Ibrahim KS, El-Sayed EM (2017) Potential renoprotective effects of rosemary and thyme against gentamicin toxicity in rats. J Diet Suppl 14(4):380–394

    Article  CAS  Google Scholar 

  • Abd-Elhakim YM, Mohammed HH, Mohamed WAM (2018) Imidacloprid impacts on neurobehavioral performance, oxidative stress, and apoptotic events in the brain of adolescent and adult rats. J Agric Food Chem 66(51):13513–13524

    Article  CAS  Google Scholar 

  • Agbohessi PT, Imorou Toko I, Houndji A, Gillardin V, Mandiki SNM, Kestemont P (2013) Acute toxicity of agricultural pesticides to embryo-larval and juvenile African catfish Clarias gariepinus. Arch Environ Contam Toxicol 64(4):692–700

  • Agius C (1981) Preliminary studies on the ontogeny of the melano-macrophages of teleost haemopoietic tissues and age-related changes. Dev Comp Immunol 5(4):597–606

    Article  CAS  Google Scholar 

  • Agius C, Roberts RJ (2003) Melano-macrophage centres and their role in fish pathology. J Fish Dis 26(9):499–509

    Article  CAS  Google Scholar 

  • Ai Q, Xu H, Mai K, Xu W, Wang J, Zhang W (2011) Effects of dietary supplementation of Bacillus subtilis and fructooligosaccharide on growth performance, survival, non-specific immune response and disease resistance of juvenile large yellow croaker, Larimichthys crocea. Aquaculture 317(1–4):155–161

  • ALsafah AH, AL-Faragi JK (2017) Influence of thyme (Thymus vulgaris) as feed additives on growth performance and antifungal activity on Saprolegnia spp. in Cyprinus carpio L. Journal of Entomology and Zoology Studies 5(6):1598–1602

  • Aly SM, Ahmed YA-G, Ghareeb AA-A, Mohamed MF (2008) Studies on Bacillus subtilis and Lactobacillus acidophilus, as potential probiotics, on the immune response and resistance of Tilapia nilotica (Oreochromis niloticus) to challenge infections. Fish & Shellfish Immunology 25(1–2):128–136

  • Annabi E, Ben Salem I, Abid-Essefi S (2019) Acetamiprid, a neonicotinoid insecticide, induced cytotoxicity and genotoxicity in PC12 cells. Toxicol Mech Methods 29(8):580–586

    Article  CAS  Google Scholar 

  • Atamaniuk TM, Kubrak OI, Husak VV, Storey KB, Lushchak VI (2014) The mancozeb-containing carbamate fungicide tattoo induces mild oxidative stress in goldfish brain, liver, and kidney. Environ Toxicol 29(11):1227–1235

    CAS  Google Scholar 

  • Azad I, 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

  • Bakke-McKellep AM, Penn MH, Salas PM, Refstie S, Sperstad S, Landsverk T, Ringo E, Krogdahl A (2007) Effects of dietary soyabean meal, inulin and oxytetracycline on intestinal microbiota and epithelial cell stress, apoptosis and proliferation in the teleost Atlantic salmon (Salmo salar L.). Br J Nutr 97(4):699–713

  • Baldissera MD, Souza CF, Golombieski JI, Seben D, Sippert LR, Salbego J, Marchesan E, Zanella R, Baldisserotto B (2018a) Purinergic signaling as potential target of thiamethoxam-induced neurotoxicity using silver catfish (Rhamdia quelen) as experimental model. Mol Cell Biochem 449(1–2):39–45

  • Baldissera MD, Souza CF, Golombieski JI, Seben D, Sippert LR, Salbego J, Zanella R, Baldisserotto B (2018b) Thiamethoxam induced hepatic energy changes in silver catfish via impairment of the phosphoryl transfer network pathway: toxicological effects on energetics homeostasis. Environ Toxicol Pharmacol 60:1–4

    Article  CAS  Google Scholar 

  • Baldissera MD, Souza CF, Seben D, Sippert LR, Salbego J, Marchesan E, Zanella R, Baldisserotto B, Golombieski JI (2018c) Gill bioenergetics dysfunction and oxidative damage induced by thiamethoxam exposure as relevant toxicological mechanisms in freshwater silver catfish Rhamdia quelen. Sci Total Environ 636:420–426

  • Birhanu BT, Lee J-S, Lee S-J, Choi S-H, Hossain MA, Park J-Y, Kim J-C, Suh J-W, Park S-C (2016) Immunomodulation of Lactobacillus pentosus PL11 against Edwardsiella tarda infection in the head kidney cells of the Japanese eel (Anguilla japonica). Fish & Shellfish Immunology 54:466–472

  • Bose S, Nath S, Sahana S (2011) Toxic impact of thiamethoxam on the growth performance and liver protein concentration of a freshwater fish Oreochromis niloticus (Trewavas). Indian Journal of Fundamental and Applied Life Sciences 1(4):274–280

  • Bruslé J, Anadon GG (1996) The structure and function of fish liver. In: Munshi JSD, Dutta HM (eds) Fish morphology. Science Publishers Inc., New York, pp 77–93

    Google Scholar 

  • Cattaneo R, Moraes BS, Loro VL, Pretto A, Menezes C, Sartori GMS, Clasen B, de Avila LA, Marchesan E, Zanella R (2012) Tissue biochemical alterations of Cyprinus carpio exposed to commercial herbicide containing clomazone under rice-field conditions. Arch Environ Contam Toxicol 62(1):97–106

  • Cheng CH, Yang FF, Liao SA, Miao YT, Ye CX, Wang AL, Tan JW, Chen XY (2015) High temperature induces apoptosis and oxidative stress in pufferfish (Takifugu obscurus) blood cells. J Therm Biol 53:172–179

  • Choi CY, An KW, An MI (2008) Molecular characterization and mRNA expression of glutathione peroxidase and glutathione S-transferase during osmotic stress in olive flounder (Paralichthys olivaceus). Comp Biochem Physiol A Mol Integr Physiol 149(3):330–337

  • Coulombe J, Favreau L (1963) A new simple semimicro method for colorimetric determination of urea. Clin Chem 9(1):102–108

    Article  CAS  Google Scholar 

  • Crosby EB, Bailey JM, Oliveri AN, Levin ED (2015) Neurobehavioral impairments caused by developmental imidacloprid exposure in zebrafish. Neurotoxicol Teratol 49:81–90

    Article  CAS  Google Scholar 

  • Dabrowska H, Ostaszewska T, Kamaszewski M, Antoniak A, Napora-Rutkowski L, Kopko O, Lang T, Fricke NF, Lehtonen KK (2012) Histopathological, histomorphometrical, and immunohistochemical biomarkers in flounder (Platichthys flesus) from the southern Baltic Sea. Ecotoxicol Environ Saf 78:14–21

  • David M, Kartheek RM (2015) Histopathological alterations in spleen of freshwater fish Cyprinus carpio exposed to sublethal concentration of sodium cyanide. Open Vet J 5(1):1–5

  • Demirci Ö, Güven K, Asma D, Öğüt S, Uğurlu P (2018) Effects of endosulfan, thiamethoxam, and indoxacarb in combination with atrazine on multi-biomarkers in Gammarus kischineffensis. Ecotoxicol Environ Saf 147:749–758

  • Dezfuli BS, Giari L, Lui A, Squerzanti S, Castaldelli G, Shinn AP, Manera M, Lorenzoni M (2012) Proliferative cell nuclear antigen (PCNA) expression in the intestine of Salmo trutta trutta naturally infected with an acanthocephalan. Parasit Vectors 5:198

  • Di J, Chu Z, Zhang S, Huang J, Du H, Wei Q (2019) Evaluation of the potential probiotic Bacillus subtilis isolated from two ancient sturgeons on growth performance, serum immunity and disease resistance of Acipenser dabryanus. Fish Shellfish Immunol (93): 711-719. https://doi.org/10.1016/j.fsi.2019.08.020

  • Doyen P, Bigot A, Vasseur P, Rodius F (2008) Molecular cloning and expression study of pi-class glutathione S-transferase (pi-GST) and selenium-dependent glutathione peroxidase (Se-GPx) transcripts in the freshwater bivalve Dreissena polymorpha. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 147(1):69–77

    Google Scholar 

  • Elblehi SS, El Euony OI, El-Nahas AF (2019a) Partial ameliorative effect of Moringa leaf ethanolic extract on the reproductive toxicity and the expression of steroidogenic genes induced by subchronic cadmium in male rats. Environ Sci Pollut Res Int 26(23):23306–23318

    Article  CAS  Google Scholar 

  • Elblehi SS, Hafez MH, El-Sayed YS (2019b) L-alpha-phosphatidylcholine attenuates mercury-induced hepato-renal damage through suppressing oxidative stress and inflammation. Environ Sci Pollut Res Int 26(9):9333–9342

    Article  CAS  Google Scholar 

  • Elblehi SS, El Euony OI, El-Sayed YS (2020) Apoptosis and astrogliosis perturbations and expression of regulatory inflammatory factors and neurotransmitters in acrylamide-induced neurotoxicity under omega3 fatty acids protection in rats. Neurotoxicology 76:44–57

    Article  CAS  Google Scholar 

  • Ellis AE (1990) Lysozyme assays. In: Stolen JS, Fletcher TC, Anderson DP, Roberson BS, Van Muiswinkel WB (eds) Techniques in fish immunology. SOS Publications, Fair Haven, pp 101–103

    Google Scholar 

  • El-Newary SA, Shaffie NM, Omer EA (2017) The protection of Thymus vulgaris leaves alcoholic extract against hepatotoxicity of alcohol in rats. Asian Pac J Trop Med 10(4):361–371

  • Abd El-Hack ME, Alagawany M, Ragab Farag M, Tiwari R, Karthik K, Dhama K, Zorriehzahra J, Adel M (2016) Beneficial impacts of thymol essential oil on health and production of animals, fish and poultry: a review. J Essent Oil Res 28(5):365–382

  • Fournie JW, Summers JK, Courtney LA, Engle VD, Blazer VS (2001) Utility of splenic macrophage aggregates as an indicator of fish exposure to degraded environments. J Aquat Anim Health 13(2):105–116

    Article  Google Scholar 

  • Franco R, Sanchez-Olea R, Reyes-Reyes EM, Panayiotidis MI (2009) Environmental toxicity, oxidative stress and apoptosis: menage a trois. Mutat Res 674(1–2):3–22

    Article  CAS  Google Scholar 

  • Galagarza OA, Smith SA, Drahos DJ, Eifert JD, Williams RC, Kuhn DD (2018) Modulation of innate immunity in Nile tilapia (Oreochromis niloticus) by dietary supplementation of Bacillus subtilis endospores. Fish & Shellfish Immunology 83:171–179

  • Geng X, Dong X-H, Tan B-P, Yang Q-H, Chi S-Y, Liu H-Y, Liu X-Q (2011) Effects of dietary chitosan and Bacillus subtilis on the growth performance, non-specific immunity and disease resistance of cobia, Rachycentron canadum. Fish & Shellfish Immunology 31(3):400–406

  • Georgieva E, Stoyanova S, Velcheva I, Yancheva V (2014) Histopathological alterations in common carp (Cyprinus carpio L.) gills caused by thiamethoxam. Braz Arch Biol Technol 57(6):991–996

    Article  CAS  Google Scholar 

  • Ghiasi F, Mirzargar SS, Badakhshan H, Shamsi S (2010) Effects of low concentration of cadmium on the level of lysozyme in serum, leukocyte count and phagocytic index in Cyprinus carpio under the wintering conditions. J Fish Aquat Sci 5(2):113–119

    Article  CAS  Google Scholar 

  • Gültepe N, Bilen S, Yılmaz S, Güroy D, Aydın S (2014) Effects of herbs and spice on health status of tilapia (Oreochromis mossambicus) challenged with Streptococcus iniae. Acta Vet Brno 83(2):125–131

    Article  CAS  Google Scholar 

  • Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione-S-transferases the first enzymatic step in mercapturic acid formation. J Biol Chem 249(22):7130–7139

    CAS  Google Scholar 

  • Harabawy ASA, Ibrahim ATA (2014) Sublethal toxicity of carbofuran pesticide on the African catfish Clarias gariepinus (Burchell, 1822): hematological, biochemical and cytogenetic response. Ecotoxicol Environ Saf 103:61–67

    Article  CAS  Google Scholar 

  • Hart LJ, Smith SA, Smith BJ, Robertson J, Holladay SD (1997) Exposure of tilapian fish to the pesticide lindane results in hypocellularity of the primary hematopoietic organ (pronephros) and the spleen without altering activity of phagocytic cells in these organs. Toxicology 118(2–3):211–221

    Article  CAS  Google Scholar 

  • Hong S, Peddie S, Campos-Pérez JJ, Zou J, Secombes CJ (2003) The effect of intraperitoneally administered recombinant IL-1β on immune parameters and resistance to Aeromonas salmonicida in the rainbow trout (Oncorhynchus mykiss). Developmental & Comparative Immunology 27(9):801–812

    Article  CAS  Google Scholar 

  • Hoseini SM, Yousefi M (2019) Beneficial effects of thyme (Thymus vulgaris) extract on oxytetracycline-induced stress response, immunosuppression, oxidative stress and enzymatic changes in rainbow trout (Oncorhynchus mykiss). Aquac Nutr 25(2):298–309

  • Jensch-Junior BE, Pressinotti LN, Borges JCS, da Silva JRMC (2006) Characterization of macrophage phagocytosis of the tropical fish Prochilodus scrofa (Steindachner, 1881). Aquaculture 251(2–4):509–515

  • Jin Y, Zheng S, Pu Y, Shu L, Sun L, Liu W, Fu Z (2011) Cypermethrin has the potential to induce hepatic oxidative stress, DNA damage and apoptosis in adult zebrafish (Danio rerio). Chemosphere 82(3):398–404

    Article  CAS  Google Scholar 

  • Karmakar R, Kulshrestha G (2009) Persistence, metabolism and safety evaluation of thiamethoxam in tomato crop. Pest Management Science: formerly Pesticide Science 65(8):931–937

    Article  CAS  Google Scholar 

  • Kawahara E, Ueda T, Nomura S (1991) In vitro phagocytic activity of white-spotted char blood cells after injection with Aeromonas salmonicida extracellular products. Fish Pathology 26(4):213–214

    Article  Google Scholar 

  • Khaldoun-Oularbi H, Bouzid N, Boukreta S, Makhlouf C, Derriche F, Djennas N (2017) Thiamethoxam Actara((R)) induced alterations in kidney liver cerebellum and hippocampus of male rats. J Xenobiot 7(1):7149

    Article  CAS  Google Scholar 

  • Kono T, Korenaga H, Sakai M (2011) Genomics of fish IL-17 ligand and receptors: a review. Fish & Shellfish Immunology 31(5):635–643

    Article  CAS  Google Scholar 

  • Kranz H, Gercken J (1987) Effects of sublethal concentrations of potassium dichromate on the occurrence of splenic melano-macrophage centres in juvenile plaice, Pleuronectes platessa, L. Journal of Fish Biology 31(sa):75–80

    Article  CAS  Google Scholar 

  • Kumar R, Mukherjee SC, Prasad KP, Pal AK (2006) Evaluation of Bacillus subtilis as a probiotic to Indian major carp Labeo rohita (Ham.). Aquac Res 37(12):1215–1221

  • Kumar R, Mukherjee S, Ranjan R, Nayak S (2008) Enhanced innate immune parameters in Labeo rohita (Ham.) following oral administration of Bacillus subtilis. Fish & Shellfish Immunology 24(2):168–172

  • Kumar VA, Janaiah C, Venkateshwarlu P (2010a) Effect of thiamethoxam alters serum biochemical parameters in Channa punctatus (Bloch). Asian Journal of Bio Science 5(1):106–110

    CAS  Google Scholar 

  • Kumar VA, Janaiah C, Venkateshwarlu P (2010b) Impact of thiamethoxam on proteases, aminases and glutamate dehydrogenase in some tissues of freshwater fish, Channa punctatus (Bloch). An Int J Life Sci 5(1):135–137

  • Kurtović B, Teskeredžić ET, Teskeredžić Z (2008) Histological comparison of spleen and kidney tissue from farmed and wild European sea bass (Dicentrarchus labrax L.). Acta Adriat 49(2):147–154

    Google Scholar 

  • Larsen K (1972) Creatinine assay by a reaction-kinetic principle. Clin Chim Acta 41:209–217

    Article  CAS  Google Scholar 

  • Lee S, Katya K, Hamidoghli A, Hong J, Kim D-J, Bai SC (2018) Synergistic effects of dietary supplementation of Bacillus subtilis WB60 and mannanoligosaccharide (MOS) on growth performance, immunity and disease resistance in Japanese eel, Anguilla japonica. Fish & Shellfish Immunology 83:283–291

  • Li C, Zhao Y, Liu T, Huang J, Zhang Q, Liu B, Xiao S, Wang H, Liu B, Wang J (2018) The distribution and function characterization of the i type lysozyme from Apostichopus japonicus. Fish & Shellfish Immunology 74:419–425

    Article  CAS  Google Scholar 

  • Liu C-H, Chiu C-H, Wang S-W, Cheng W (2012) Dietary administration of the probiotic, Bacillus subtilis E20, enhances the growth, innate immune responses, and disease resistance of the grouper, Epinephelus coioides. Fish & Shellfish Immunology 33(4):699–706

  • Liu H, Wang S, Cai Y, Guo X, Cao Z, Zhang Y, Liu S, Yuan W, Zhu W, Zheng Y (2017) Dietary administration of Bacillus subtilis HAINUP40 enhances growth, digestive enzyme activities, innate immune responses and disease resistance of tilapia, Oreochromis niloticus. Fish & Shellfish Immunology 60:326–333

  • Liu X, Zhang Q, Li S, Mi P, Chen D, Zhao X, Feng X (2018) Developmental toxicity and neurotoxicity of synthetic organic insecticides in zebrafish (Danio rerio): a comparative study of deltamethrin, acephate, and thiamethoxam. Chemosphere 199:16–25

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  • Magare SR, Patil HT (2000) Effect of pesticides on oxygen consumption, red blood cell count and metabolites of a fish, Puntius ticto. Environ Ecology 18:891–894

    CAS  Google Scholar 

  • Matsche M (2011) Evaluation of tricaine methanesulfonate (MS-222) as a surgical anesthetic for Atlantic sturgeon Acipenser oxyrinchus oxyrinchus. J Appl Ichthyol 27(2):600–610

  • Mela M, Guiloski IC, Doria HB, Randi MA, de Oliveira Ribeiro CA, Pereira L, Maraschi AC, Prodocimo V, Freire CA, Silva de Assis HC (2013) Effects of the herbicide atrazine in neotropical catfish (Rhamdia quelen). Ecotoxicol Environ Saf 93:13–21

  • Modesto KA, Martinez CB (2010) Roundup® causes oxidative stress in liver and inhibits acetylcholinesterase in muscle and brain of the fish Prochilodus lineatus. Chemosphere 78(3):294–299

    Article  CAS  Google Scholar 

  • Mohany M, El-Feki M, Refaat I, Garraud O, Badr G (2012) Thymoquinone ameliorates the immunological and histological changes induced by exposure to imidacloprid insecticide. J Toxicol Sci 37(1):1–11

    Article  CAS  Google Scholar 

  • Montero, D., Izquierdo, M. S., Tort, L., Robaina, L., & Vergara, J. M. (1999). High stocking density produces crowding stress altering some physiological and biochemical parameters in gilthead seabream, Sparus aurata, juveniles. Fish Physiology and Biochemistry, 20(1), 53-60.‏

  • Navarrete, P., Toledo, I., Mardones, P., Opazo, R., Espejo, R., & Romero, J. (2010). Effect of Thymus vulgaris essential oil on intestinal bacterial microbiota of rainbow trout, Oncorhynchus mykiss (Walbaum) and bacterial isolates. Aquaculture Research, 41(10), e667-e678.‏

  • Norbury CJ, Hickson ID (2001) Cellular responses to DNA damage. Annu Rev Pharmacol Toxicol 41:367–401

    Article  CAS  Google Scholar 

  • Oliveira M, Maria V, Ahmad I, Serafim A, Bebianno M, Pacheco M, Santos M (2009) Contamination assessment of a coastal lagoon (Ria de Aveiro, Portugal) using defence and damage biochemical indicators in gill of Liza aurata—an integrated biomarker approach. Environ Pollut 157(3):959–967

    Article  CAS  Google Scholar 

  • Oliveira SE, Costa PM, Nascimento SB, Castro WV, Ribeiro R, Santos HB, Thome RG (2018) Atrazine promotes immunomodulation by melanomacrophage centre alterations in spleen and vascular disorders in gills from Oreochromis niloticus. Aquat Toxicol 202:57–64

    Article  CAS  Google Scholar 

  • Ozdemir S, Altun S, Arslan H (2018) Imidacloprid exposure cause the histopathological changes, activation of TNF-alpha, iNOS, 8-OHdG biomarkers, and alteration of caspase 3, iNOS, CYP1A, MT1 gene expression levels in common carp (Cyprinus carpio L.). Toxicol Rep 5:125–133

  • Pereira Navarro Lins JA, Gaberz Kirschnik P, Da Silva Queiroz V, Maris Cirio S (2010) Uso de peixes como biomarcadores para monitoramento ambiental aquático. Revista Acadêmica: Ciência Animal 8(4):469

    Article  Google Scholar 

  • Pronina SV, Batueva MDD, Pronin NM (2014) Characteristics of melanomacrophage centers in the liver and spleen of the roach Rutilus rutilus (Cypriniformes: Cyprinidae) in Lake Kotokel during the Haff disease outbreak. J Ichthyol 54(1):104–110

  • Qiao Q, Liang H, Zhang X (2013) Effect of cyanobacteria on immune function of crucian carp (Carassius auratus) via chronic exposure in diet. Chemosphere 90(3):1167–1176

    Article  CAS  Google Scholar 

  • Reda RM, El-Hady M, Selim KM, El-Sayed HM (2018) Comparative study of three predominant gut Bacillus strains and a commercial B. amyloliquefaciens as probiotics on the performance of Clarias gariepinus. Fish & Shellfish Immunology 80:416–425

  • Reed LJ, Muench H (1938) A simple method of estimating fifty per cent endpoints. Am J Epidemiol 27(3):493–497

    Article  Google Scholar 

  • Reitman S, Frankel S (1957) A colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases. Am J Clin Pathol 28(1):56–63

    Article  CAS  Google Scholar 

  • Ribeiro HJ, Procopio MS, Gomes JM, Vieira FO, Russo RC, Balzuweit K, Chiarini-Garcia H, Castro AC, Rizzo E, Correa JD Jr (2011) Functional dissimilarity of melanomacrophage centres in the liver and spleen from females of the teleost fish Prochilodus argenteus. Cell Tissue Res 346(3):417–425

    Article  CAS  Google Scholar 

  • Rota MC, Herrera A, Martínez RM, Sotomayor JA, Jordán MJ (2008) Antimicrobial activity and chemical composition of Thymus vulgaris, Thymus zygis and Thymus hyemalis essential oils. Food Control 19(7):681–687

  • Sales CF, Santos K, Rizzo E, Ribeiro R, Santos HBD, Thome RG (2017) Proliferation, survival and cell death in fish gills remodeling: from injury to recovery. Fish Shellfish Immunol 68:10–18

    Article  Google Scholar 

  • Sarasquete C, Ortiz JB, González de Canales ML (2007) Histopathological changes induced by lindane (γ-HCH) in various organs of fishes. Sci Mar 67(1):53–61

    Article  Google Scholar 

  • Sayed AH, Younes HAM (2017) Melanomacrophage centers in Clarias gariepinus as an immunological biomarker for toxicity of silver nanoparticles. J Microsc Ultrastruct 5(2):97–104

  • Siwicki A, Studnicka M (1987) The phagocytic ability of neutrophils and serum lysozyme activity in experimentally infected carp, Cyprinus carpio L. Journal of Fish Biology 31(sa):57–60

  • Sönmez AY, Bilen S, Alak G, Hisar O, Yanık T, Biswas G (2015) 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(1):165–175

    Article  CAS  Google Scholar 

  • Steinel NC, Bolnick DI (2017) Melanomacrophage centers as a histological Indicator of immune function in fish and other poikilotherms. Front Immunol 8:827

    Article  CAS  Google Scholar 

  • Stoyanova S, Georgieva E, Velcheva I, Yancheva V, Atanasova P (2012) Effects of the insecticide “Actara 25 WG” on the glyconeogenesis in the liver of common carp (Cyprinus carpio L.). Journal of BioScience & Biotechnology 1(3):249–254

    Google Scholar 

  • Stoyanova S, Yancheva V, Velcheva I, Atanasova P, Georgieva E (2015) Thiamethoxam causes histochemical changes in the liver of Aristichthys nobilis Rich., 1845. J BioSci Biotechnol 4(3): 321-325.

  • Stoyanova S, Yancheva V, Iliev I, Vasileva T, Bivolarski V, Velcheva I, Georgieva E (2016) Biochemical, histological and histochemical changes in Aristichthys nobilis Rich. liver exposed to thiamethoxam. Period Biol 118(1):29–36

    Article  Google Scholar 

  • Stoyanova S, Georgieva E, Velcheva I, Atanasova P, Yancheva V (2019) Lipid accumulation in Cyprinus carpio (Linnaeus, 1785) liver induced by thiamethoxam. ZooNotes (136-141), p1-4.

  • Sun Y-Z, Yang H-L, Ma R-L, Lin W-Y (2010) Probiotic applications of two dominant gut Bacillus strains with antagonistic activity improved the growth performance and immune responses of grouper Epinephelus coioides. Fish & Shellfish Immunology 29(5):803–809

  • Sunyer JO (2013) Fishing for mammalian paradigms in the teleost immune system. Nat Immunol 14(4):320–326

    Article  CAS  Google Scholar 

  • Suresh N (2009) Effect of cadmium chloride on liver, spleen and kidney melano macrophage centres in Tilapia mossambica. J Environ Biol 30(4):505–508

    CAS  Google Scholar 

  • Tang L, Huang K, Xie J, Yu D, Sun L, Huang Q, Bi Y (2017) 1-Deoxynojirimycin from Bacillus subtilis improves antioxidant and antibacterial activities of juvenile Yoshitomi tilapia. Electron J Biotechnol 30:39–47

    Article  CAS  Google Scholar 

  • Thany SH (2011) Thiamethoxam, a poor agonist of nicotinic acetylcholine receptors expressed on isolated cell bodies, acts as a full agonist at cockroach cercal afferent/giant interneuron synapses. Neuropharmacology 60(4):587–592

    Article  CAS  Google Scholar 

  • Tietz N, Burtis C, Duncan P, Ervin K, Petitclerc C, Rinker A, Shuey D, Zygowicz E (1983) A reference method for measurement of alkaline phosphatase activity in human serum. Clin Chem 29(5):751–761

    Article  CAS  Google Scholar 

  • Uchiyama M, Mihara M (1978) Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 86(1):271–278

    Article  CAS  Google Scholar 

  • Uğurlu P, Ünlü E, Satar EI (2015) The toxicological effects of thiamethoxam on Gammarus kischineffensis (Schellenberg 1937) (Crustacea: Amphipoda). Environ Toxicol Pharmacol 39(2):720–726

    Article  CAS  Google Scholar 

  • Vincent S, Sumit R, Bavithra S, Victoria V, Akhila N, Prabha J (2019) Metallothionein induced time dependent histomorphometric analysis of Clarias gariepinus exposed to cadmium. Bull Environ Contam Toxicol 102(1):32–38

  • Wang X, Xing H, Jiang Y, Wu H, Sun G, Xu Q, Xu S (2013) Accumulation, histopathological effects and response of biochemical markers in the spleens and head kidneys of common carp exposed to atrazine and chlorpyrifos. Food Chem Toxicol 62:148–158

    Article  CAS  Google Scholar 

  • Wang Y, Zhang Y, Li W, Han Y, Guo B (2019) Study on neurotoxicity of dinotefuran, thiamethoxam and imidacloprid against Chinese lizards (Eremias argus). Chemosphere 217:150–157

  • Yan F-J, Tian X-L, Dong S-L, Fang Z-H, Yang G (2014) Growth performance, immune response, and disease resistance against Vibrio splendidus infection in juvenile sea cucumber Apostichopus japonicus fed a supplementary diet of the potential probiotic Paracoccus marcusii DB11. Aquaculture 420-421:105–111

    Article  CAS  Google Scholar 

  • Yan SH, Wang JH, Zhu LS, Chen AM, Wang J (2016) Thiamethoxam induces oxidative stress and antioxidant response in zebrafish (Danio rerio) livers. Environ Toxicol 31(12):2006–2015

    Article  CAS  Google Scholar 

  • Yin Y, Zhang P, Yue X, Du X, Li W, Yin Y, Yi C, Li Y (2018) Effect of sub-chronic exposure to lead (Pb) and Bacillus subtilis on Carassius auratus gibelio: bioaccumulation, antioxidant responses and immune responses. Ecotoxicol Environ Saf 161:755–762

  • Yin Y, Yue X, Zhang D, Zhang P, Abdallah A, Yin Y, Cai Y, Li Y (2019) Study of bioaccumulation, hematological parameters, and antioxidant responses of Carassius auratus gibelio exposed to dietary lead and Bacillus subtilis. Biol Trace Elem Res 189(1):233–240

  • Young T-H, Kao C-Y, Hsieh M-Y, Wang B-J, Hsu J-P (2001) Electrophoretic properties of latex particles with immobilized bovine serum albumin. J Colloid Interface Sci 239(2):563–567

    Article  CAS  Google Scholar 

  • Zadmajid V, Mohammadi C (2017) Dietary thyme essential oil (Thymus vulgaris) changes serum stress markers, enzyme activity, and hematological parameters in gibel carp (Carassius auratus gibelio) exposed to silver nanoparticles. Iran J Fish Sci 16(3):1063–1084

  • Zahran E, Risha E, Awadin W, Palic 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 

  • Zaineldin AI, Hegazi S, Koshio S, Ishikawa M, Bakr A, El-Keredy AM, Dawood MA, Dossou S, Wang W, Yukun Z (2018) Bacillus subtilis as probiotic candidate for red sea bream: growth performance, oxidative status, and immune response traits. Fish & Shellfish Immunology 79:303–312

    Article  CAS  Google Scholar 

  • Zargar A, Rahimi-Afzal Z, Soltani E, Taheri Mirghaed A, Ebrahimzadeh-Mousavi HA, Soltani M, Yuosefi P (2019) Growth performance, immune response and disease resistance of rainbow trout (Oncorhynchus mykiss) fed Thymus vulgaris essential oils. Aquac Res

  • Zhang Q, Yu H, Tong T, Tong W, Dong L, Xu M, Wang Z (2014) Dietary supplementation of Bacillus subtilis and fructooligosaccharide enhance the growth, non-specific immunity of juvenile ovate pompano, Trachinotus ovatus and its disease resistance against Vibrio vulnificus. Fish & Shellfish Immunology 38(1):7–14

  • Zhao Y, Zhang W, Xu W, Mai K, Zhang Y, Liufu Z (2012) Effects of potential probiotic Bacillus subtilis T13 on growth, immunity and disease resistance against Vibrio splendidus infection in juvenile sea cucumber Apostichopus japonicus. Fish & Shellfish Immunology 32(5):750–755

  • Zhou S, Song D, Zhou X, Mao X, Zhou X, Wang S, Wei J, Huang Y, Wang W, Xiao S-M (2019) Characterization of Bacillus subtilis from gastrointestinal tract of hybrid Hulong grouper (Epinephelus fuscoguttatus × E. lanceolatus) and its effects as probiotic additives. Fish & Shellfish Immunology 84:1115–1124

  • Zhu L, Li W, Zha J, Li N, Wang Z (2019) Chronic thiamethoxam exposure impairs the HPG and HPT axes in adult Chinese rare minnow (Gobiocypris rarus): docking study, hormone levels, histology, and transcriptional responses. Ecotoxicol Environ Saf 185:109683

Download references

Acknowledgments

All authors would like to thank the Faculties of Veterinary Medicine at Alexandria and Damanhour Universities for their facilities offered to finalize this research work. This project was funded by the Researchers Supporting Project number (RSP-2019/121), King Saud University, Riyadh, Saudi Arabia.

Funding

This project was funded by the Researchers Supporting Project number (RSP-2019/121), King Saud University, Riyadh, Saudi Arabia.

Author information

Authors and Affiliations

  1. Department of Forensic Medicine and Toxicology, Faculty of Veterinary Medicine, Alexandria University, Edfina, Beheira, 22758, Egypt

    Omnia I. El Euony

  2. Department of Pathology, Faculty of Veterinary Medicine, Alexandria University, Edfina, Beheira, 22758, Egypt

    Samar S. Elblehi

  3. Department of Poultry and Fish Diseases, Faculty of Veterinary Medicine, Alexandria University, Edfina, Beheira, 22758, Egypt

    Hany M. Abdel-Latif

  4. Department of Zoology, College of Science, King Saud University, P.O. Box 2455, Riyadh, 11451, Saudi Arabia

    Mohamed M. Abdel-Daim

  5. Pharmacology Department, Faculty of Veterinary Medicine, Suez Canal University, Ismailia, 41522, Egypt

    Mohamed M. Abdel-Daim

  6. Department of Forensic Medicine and Toxicology, Faculty of Veterinary Medicine, Damanhour University, Damanhour, 22511, Egypt

    Yasser S. El-Sayed

Authors
  1. Omnia I. El Euony
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Samar S. Elblehi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hany M. Abdel-Latif
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mohamed M. Abdel-Daim
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yasser S. El-Sayed
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yasser S. El-Sayed.

Ethics declarations

The experimental methodology, design protocol, and rearing of fish were approved and conducted according to the Experimental Animal Use and Ethics Committee at the Faculty of Veterinary Medicine, Alexandria University, Egypt.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible editor: Philippe Garrigues

Publisher’s note

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

Electronic supplementary material

ESM 1

(DOCX 24 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

El Euony, O.I., Elblehi, S.S., Abdel-Latif, H.M. et al. Modulatory role of dietary Thymus vulgaris essential oil and Bacillus subtilis against thiamethoxam-induced hepatorenal damage, oxidative stress, and immunotoxicity in African catfish (Clarias garipenus). Environ Sci Pollut Res 27, 23108–23128 (2020). https://doi.org/10.1007/s11356-020-08588-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-08588-5

Keywords

Search

Navigation