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Effect of Silymarin Supplementation on Nickel Oxide Nanoparticle Toxicity to Rainbow Trout (Oncorhynchus mykiss) Fingerlings: Pancreas Tissue Histopathology and Alkaline Protease Activity

Abstract

The effects of dietary nickel oxide nanoparticles (NiO-NPs) contamination along with silymarin supplementation on pancreatic tissue of rainbow trout fingerlings were investigated. Five treatments including different levels of NiO-NPs (0, 100 and 500 mg kg−1 feed) and silymarin (0 and 1 g kg−1 feed) in three respective replicates were designed. The trial was conducted under 12L:12D photoperiod condition for 60 days. Tissue samples for histological and enzymatic studies were taken on days 30 and 60. The results from day 30 indicated that the highest and lowest alkaline protease activities were belonged to fish fed diet without any nanoparticles (T1) and those fed 100 or 500 mg kg−1 feed (T4 and T5), respectively. Dietary silymarin could to some extent prevent toxic effects of NiO-NPs on enzyme activity (T2 vs. T3). Acinar cells necrosis, edema of connective tissue and cellular shrinkage were observed in NiO-NPs received groups (T4 and T5). At the end of the trial, T2 and T3 could regain their digestive capacity after removal of nanoparticles and those groups continued to receive nanoparticles until the end of the trial (T4 and T5) showed the lowest alkaline protease activity. Moreover, the histological observations revealed pancreas tissue necrosis, nuclear degeneration and vascular dilation in the latter groups. In conclusion, NiO-NPs affected pancreatic tissue and its function in a dose-dependent manner, while dietary silymarin helped fish to sustain digestive capacity. Future researches should focus on the ecological outcomes of pollutants induced toxicity.

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References

  1. Agarwal M, Murugan MS, Sharma A, Rai R, Kamboj A, Sharma H, Roy SK (2013) Nanoparticles and its toxic effects: a review. Int J Curr Microbiol Appl Sci 2:76–82

    Google Scholar 

  2. Applebaum SL, Perez R, Lazo GP, Holt GL (2001) Characterization of chymotrypsin activity during ontogeny of larval red drum (Sciaenops ocellatus). Fish Physiol Biochem 25:291–300

    Article  Google Scholar 

  3. Ardestani A, Yazdanparast R, Jamshidi Sh (2008) Therapeutic effects of Teucrium polium extract on oxidative stress in pancreas of streptozotocin-induced diabetic rats. J Med Food 11:525–532

    Article  Google Scholar 

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

    Google Scholar 

  5. Bauer DH, Lee DJ, Sinnhuber RO (1969) Acute toxicity of aflatoxins B1 and G1 in the rainbow trout (Salmo gairdneri). Toxicol Appl Pharmacol 15:415–419

    Article  Google Scholar 

  6. Bolasina S, Perez A, Yamashita Y (2006) Digestive enzymes activity during ontogenic development and effect of starvation in Japanese flounder, Paralichthys olivaceus. Aquaculture 252:503–515

    Article  Google Scholar 

  7. Boujard T, Burel C, Médale F, Haylor G, Moisan A (2000) Effect of past nutritional history and fasting on feed intake and growthin rainbow trout Oncorhynchus mykiss. Aquat Living Resour 13(03):129–137

    Article  Google Scholar 

  8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  Google Scholar 

  9. Brown CC, Baker DC, Barker IK (2007) Intestine. In: Jubb K, Palmer’s Pathology of Domestic Animals (5th Edition) Vol. 2, edited by M Grant Maxie, Elsevier, Edinburgh, pp 69–128

  10. Charles JA (2007) Exocrine pancreas. In: Jubb K, Palmer’s Pathology of Domestic Animals (5th Edition) Vol. 2, edited by M Grant Maxie, Elsevier, Edinburgh, pp 389–408

  11. Chavez-Sanchez MC, Palacios CM, Moreno IO (1994) Pathological effects of feeding young Oreochromis niloticus diets supplemented with different levels of aflatoxin B1. Aquaculture 127:49–60

    Article  Google Scholar 

  12. Chong ASC, Hashim R, Lee CY, Ali BA (2002) Partial characterization and activities of proteases form the digestive tract of discus fish (Symphysodon aequifasciata). Aquaculture 203:321–333

    Article  Google Scholar 

  13. Corring T (1980) The adaptations of digestive enzymes to the diet: its physiological significance. Reprod Nutr Dév. 20(4B):1217–1235

    Article  Google Scholar 

  14. Dedourge-Geffard O, Palais F, Biagianti-Risbourg S, Geffard O, Geffard A (2009) Effects of metals on feeding rate and digestive enzymes in Gammarus fossarum: an in situ experiment. Chemosphere 77:1569–1576

    Article  Google Scholar 

  15. Doronicheva N, Yasui H, Sakurai H (2007) Chemical structure-dependent differential effects of flavonoids on the catalase activity as evaluated by a chemiluminescent method. Biol Pharm Bull 30:213–217

    Article  Google Scholar 

  16. Eisele TA, Sinnhuber RO, Nixon JE (1983) Dietary antioxidant effects on the hepatic mixed-function oxidase system of rainbow trout (Salmo gairdneri). Food Chem Toxicol 21:273–277

    Article  Google Scholar 

  17. Federici G, Shaw BJ, Handy RD (2007) Toxicity of titanium dioxide nanoparticles to rainbow trout (Oncorhynchus mykiss): gill injury, oxidative stress, and other physiological effects. Aquat Toxicol 84:415–430

    Article  Google Scholar 

  18. Ferraris RP, Tan JD, DeLaCruz MC (1987) Development of the digestive tract of milkfish, Chanos chanos (Forsskal): histology and histochemistry. Aquaculture 61:241–257

    Article  Google Scholar 

  19. Filippov AA, Golovanova IL, Aminov AI (2013) Effects of organic pollutants on fish digestive enzymes: a review. Inland Water Biol 6:155–160

    Article  Google Scholar 

  20. Garcia-Carreno FL, Haard NF (1993) Characterization of proteinase classes in Langostilla pleuroncodesplanipes and Crayfish Pacifastacus astacus extracts. J Food Biochem 17:97–113

    Article  Google Scholar 

  21. Grenier B, Applegate TJ (2013) Modulation of intestinal functions following mycotoxin ingestion: meta-analysis of published experiments in animals. Toxins 5:396–430

    Article  Google Scholar 

  22. Han XY, Huang QC, Li WF, Jiang JF, Xu ZR (2008) Changes in growth performance, digestive enzyme activities and nutrient digestibility of cherry valley ducks in response to aflatoxin B1 levels. Livest Sci 119:216–220

    Article  Google Scholar 

  23. Hanhineva K, Torronen R, Bondia-Pons I, Pekkine J, Kolehmainen M, Mykkanen H, Poutanen K (2010) Impact of dietary polyphenols on carbohydrate metabolism. Int J Mol Sci 11:1365–1402

    Article  Google Scholar 

  24. Hsieh MS, Yin LJ, Jiang ST (2008) Purification and characterization of the amylase from a small abalone Haliotis sieboldii. Fish Sci 74:425–432

    Article  Google Scholar 

  25. Imani A, Yazdanparast R, Farhangi M, Bakhtiyari M, Saljoghi ZS (2009) Effect of different food deprivation periods on digestive enzyme activities of rainbow trout Oncorhynchus mykiss. In: Moksness E, Dahl E, Støttrup J (eds). Aquaculture Eroupe 2009 Torndheim, pp 191–192

  26. Ispas C, Andreescu D, Patel A, Goia DV, Andreescu S, Wallace KN (2009) Toxicity and developmental defects of different sizes and shape of nickel nanoparticles in zebrafish. Environ Sci Technol 43:6349–6356

    Article  Google Scholar 

  27. Jantrarotai W, Lovell RT, Grizzle JM (1990) Acute toxicity of aflatoxin B1 to channel catfish. J Aquat Anim Health 2:237–247

    Article  Google Scholar 

  28. Ji SC, Takaoka O, Lee SW, Hwang JH, Kim YS, Ishimura K, Seoka M, Jeong GS, Takii K (2009) Effect of dietary medicinal herbs on lipid metabolism and stress recovery in red sea bream Pagrus major. Fish Sci 75:665–672

    Article  Google Scholar 

  29. Jia R, Cao L, Du J, Xu P, Jeney G, Yin G (2013) The protective effect of silymarin on the carbon tetrachloride (CCl4)-induced liver injury in common carp (Cyprinus carpio). In Vitro Cell Dev Biol Anim 49:155–161

    Article  Google Scholar 

  30. Jobling M (1995) Digestion and absorption. Environmental biology of fishes. Chapman and Hall, London, pp 175–210

    Google Scholar 

  31. Kannan K, Jain SK (2004) Effect of vitamin B6 on oxygen radicals, mitochondrial membrane potential, and lipid peroxidation in H2O2-treated U937 monocytes. Free Radic Biol Med 36:423–428

    Article  Google Scholar 

  32. Karkanis A, Bilalis D, Efthimiadou A (2011) Cultivation of milk thistle (Silybum marianum L. Gaertn.), a medicinal weed. Ind Crops Prod 34:825–830

    Article  Google Scholar 

  33. Kharat PS, Pathan TS, Shejule KB (2014) Histopatholocal changes in hepatopancreas of freshwater prawn, Macrobrachium Kistnensis exposed to TBTCL. Middle East J Sci Res 22:1396–1400

    Google Scholar 

  34. Kim S, Choi JE, Choi J, Chung KH, Park K, Yi J, Ryu DY (2009) Oxidative stress-dependent toxicity of silver nanoparticles in human hepatoma cells. Toxicol In Vitro 23:1076–1084

    Article  Google Scholar 

  35. Kovriznych JA, Sotnikova R, Zeljenkova D, Rollerova E, Szabova E (2014) Long-term (30 days) toxicity of NiO nanoparticles for adult zebrafish (Danio rerio). Interdiscip Toxicol 7:23–26

    Article  Google Scholar 

  36. Kumar Sharma A, Bharti S, Ojha S, Bhatia J, Kumar N, Ray R, Kumari S, Arya DS (2011) Up-regulation of PPARg, heat shock protein-27 and -72 by naringin attenuates insulin resistance, b-cell dysfunction, hepatic steatosis and kidney damage in a rat model of type 2 diabetes. Br J Nutr 106(11):1713–1723

  37. Le Bihan E, Perrin A, Koueta N (2004) Development of a bioassay from isolated digestive gland cells of the cuttlefish Sepia officinalis L. (Mollusca Cephalopoda): effect of Cu, Zn and Ag on enzyme activities and cell viability. J Exp Mar Biol Ecol 309:47–66

    Article  Google Scholar 

  38. Lemieux H, Blier P, Dutil J (1999) Do digestive enzymes set a physiological limit on growth rate and food conversion efficiency in the Atlantic cod (Gadus morhua). Fish Physiol Biochem 20:293–303

    Article  Google Scholar 

  39. Li SJ, Li JL, Wu TT (2007) The effects of copper, iron and zinc on digestive enzyme activities in the hybrid tilapia Oreochromis niloticus (L.) × Oreochromis aureus (Steindachner). J Fish Biol 71:1788–1798

    Article  Google Scholar 

  40. Lovell RT (2003) Diet and fish husbandry. In: Halver JE, Hardy RW (eds) Fish nutrition, 3rd edn. Academic Press, San Diego, pp 703–754

    Chapter  Google Scholar 

  41. Malekinejad H, Alizadeh A, Cheraghi H, Meshkin S, Dardmeh F (2012) The protective effect of liquorice plant extract on CCl4-induced hepatotoxicity in common carp (Cyprinus carpio). Vet Res Forum 1:158–164

    Google Scholar 

  42. McWilliams SR, Karasov WH (2001) Phenotypic flexibility in digestive system structure and function in migratory birds and its ecological significance: a review. Comp Biochem Physiol A Mol Integr Physiol 128(3):577–591

    Article  Google Scholar 

  43. Rather MA, Sharma R, Aklakur A, Ahmad S, Kumar N, Khan M, Ramya VL (2011) Nanotechnology: a novel tool for aquaculture and fisheries development. A prospective mini-review. Fish Aquac J 16:1–5

  44. Reddy PS, Fingerman M (1994) Effect of cadmium chloride on amylase activity in the red swamp crayfish, Procambarus clarkii. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 109:309–314

    Article  Google Scholar 

  45. Rungraungsak-Torrissen K (2007) Digestive efficiency, growth and qualities of muscle and oocyte in Atlantic salmon (Salmo salar L.) fed with krill meal as an alternative protein source. J Food Biochem 31:509–540

    Article  Google Scholar 

  46. Rungraungsak-Torrissen K, Lied E, Espe M (1994) Differences in digestion and absorption of dietary protein in Atlantic salmon (Salmo salar) with genetically different trypsin isozymes. J Fish Biol 45:1087–1104

    Article  Google Scholar 

  47. Rungruangsak-Torrissen K (2012) Trypsin and its implementations for growth, maturation, and dietary quality assessment. In: Weaver k, Kelley C (eds) Trypsin: Structure, Biosynthesis and Functions, 1st edn. Nova Science Publishers Inc, New York, pp 1–59  

  48. Rungruangsak-Torrissen K, Thongprajukaew K, Sansuwan K, Thapthimdaeng P, Kovitvadhi U, Seetaha S, Choowongkomon K, M Beck I, O Arnøy O (2012) Ecological effects on food utilization, trypsin isozymes, and performance qualities of growth and maturation in northeast Arctic cod (Gadus morhua L.). Open Fish Sci J 5:44–56

  49. Sahoo PK, Mukherjee SC (2002) Influence of high dietary α-tocopherol intakes on specific immune response, nonspecific resistance factors and disease resistance of healthy and aflatoxin B1-induced immunocompromised Indian major carp, Labeo rohita (Hamilton). Aquac Nutr 8:159–167

    Article  Google Scholar 

  50. Samanta P, Pal S, Mukherjee AK, Senapati T, Kole D, Ghosh AR (2014) Effects of almix herbicide on profile of digestive enzymes of three freshwater teleostean fishes in rice field condition. Toxicol Rep 1:379–384

    Article  Google Scholar 

  51. Sarkar B, Kumar M, Verma S, Rhathore RM (2015) Effect of dietary nanosilver on gut proteases and general performance in zebrafish (Danio rerio). Int J Aquat Biol 3:60–67

    Google Scholar 

  52. Seebaugh DR, L’Amoreaux WJ, Wallace WG (2011) Digestive toxicity in grass shrimp collected along an impact gradient. Aquat Toxicol 105:609–617

    Article  Google Scholar 

  53. Seebaugh DR, Wallace WG, L’Amoreaux WJ, Stewart GM (2012) Carbon assimilation and digestive toxicity in naïve grass shrimp (Palaemonetes pugio) exposed to dietary cadmium. Bull Environ Contam Toxicol 88:449–455

    Article  Google Scholar 

  54. Sivaram V, Babu MM, Immanuel G, Murugadass S, Citarasu T, Marian MP (2004) Growth and immune response of juvenile greasy groupers (Epinephelus tauvina) fed with herbal antibacterial active principle supplemented diets against Vibrio harveyi infections. Aquaculture 237:9–20

    Article  Google Scholar 

  55. Škottová N, Krečman V, Šimánek V (1999) Activities of silymarin and its flavonolignans upon low density lipoprotein oxidizability in vitro. Phytother Res 13:535–537

    Article  Google Scholar 

  56. Solomon LR, Cohen K (1989) Erythrocyte oxygen transport and metabolism and effect of vitamin B6 therapy in type 2 diabetes mellitus. Diabetes 38:881–886

    Article  Google Scholar 

  57. Souza MF, Tome AR, Rao VSN (1999) Inhibition by the bioflavonoid ternatin of aflatoxin b1-induced lipid peroxidation in rat liver. J Pharm Pharmacol 51:125–129

    Article  Google Scholar 

  58. Sunde J, Taranger GL, Rungraungsak-Torrissen K (2001) Digestive protease activities and free amino acids in white muscle as indicators for feed conversion efficiency and growth rate in Atlantic salmon (Salmo salar L.). Fish Physiol Biochem 25:335–345

    Article  Google Scholar 

  59. Suzer C, Saka Ş, Firat K (2006) Effects of illumination on early life development and digestive enzyme activities in common pandora Pagellus erythrinus L. larvae. Aquaculture 260:86–93

    Article  Google Scholar 

  60. Tee JK, Ong CN, Bay BH, Ho HK, Leong DT (2015) Oxidative stress by inorganic nanoparticles. WIREs Nanomed Nanobiotechnol. doi:10.1002/wnan.1374

    Google Scholar 

  61. Valko M, Leibfritz D, Moncol J, Cronin MTD, Mazur M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39:44–84

    Article  Google Scholar 

  62. Virgili F, Marino M (2008) Regulation of cellular signals from nutritional molecules: a specific role for phytochemicals, beyond antioxidant activity. Free Radic Biol Med 45:1205–1216

    Article  Google Scholar 

  63. Wang T, Long X, Cheng Y, Liu Z, Yan S (2015) A comparison effect of copper nanoparticles versus copper sulphate on Juvenile Epinephelus coioides: growth parameters, digestive enzymes, body composition, and histology as biomarkers. Int J Genomics. doi:10.1155/2015/783021

  64. Woźny M, Dobosz S, Obremski K, Hliwa P, Gomułka P, Łakomiak A, Różyński R, Zalewski T, Brzuzan P (2015) Feed-borne exposure to zearalenone leads to advanced ovarian development and limited histopathological changes in the liver of premarket size rainbow trout. Aquaculture 448:71–81

    Article  Google Scholar 

  65. Yan T, Teo LH, Sin YM (1996) Effects of metals on α-amylase activity in the digestive gland of the green mussel, Perna viridis L. Bull Environ Contam Toxicol 56:677–682

    Article  Google Scholar 

  66. Yazdanparast R, Ardestani A, Jamshidi S (2007) Experimental diabetes treated with Achillea santolina: effect on pancreatic oxidative parameters. J Ethnopharmacol 112:13–18

    Article  Google Scholar 

  67. Zambare SP, Mahajan AY (2001) Heavy metal (copper and mercury) induced alterations in the enzyme secretory activity of hepatopancreas of a freshwater bivalve Corbicula Striatella. Pollut Res 20:143–146

    Google Scholar 

  68. Zhan XA, Li JX, Xu ZR, Wang M (2005) Effects of fluoride on pancreatic digestive enzyme activities and ultrastructure in young pigs. Fluoride 38:215

    Google Scholar 

  69. Zhang L, Wang WX (2006) Significance of subcellular metal distribution in prey in influencing the trophic transfer of metals in a marine fish. Limnol Oceanogr 51:2008–2017

    Article  Google Scholar 

  70. Zhao J, Li N, Wang S, Zhao X, Wang J, Yan J, Ruan J, Wang H, Hong F (2010) The mechanism of oxidative damage in the nephrotoxicity of mice caused by nano-anatase TiO2. J Exp Nanosci 5:447–462

    Article  Google Scholar 

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Acknowledgments

The authors would like to express their sincere gratitude to Vice-Chancellor for Research and Technology of Urmia University, I.R. Iran, for financial support of the research and also to Mr Jalili for his assistance in diet preparation and sampling. We are also thankful to staffs of Laboratory of Aquaculture, Urmia Lake Research Institute for their close collaborations during fish husbandry. We also appreciate the constructive suggestions and criticism given by two anonymous reviewers which certainly elaborated the quality of the manuscript.

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Nazdar, N., Imani, A., Noori, F. et al. Effect of Silymarin Supplementation on Nickel Oxide Nanoparticle Toxicity to Rainbow Trout (Oncorhynchus mykiss) Fingerlings: Pancreas Tissue Histopathology and Alkaline Protease Activity. Iran J Sci Technol Trans Sci 42, 353–361 (2018). https://doi.org/10.1007/s40995-016-0052-5

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Keywords

  • Pancreas
  • Alkaline protease
  • Nickel oxide nanoparticles
  • Rainbow trout