Skip to main content

Advertisement

SpringerLink
Log in

Effect of Dietary Zinc-Nanoparticles on Growth Performance, Anti-Oxidative and Immunological Status of Fish Reared Under Multiple Stressors

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Zinc is one of the essential micronutrients that can be obtained via water and diet in aquatic animals to meet their physiological needs. The present study was designed to understand the effect of the supplementation of zinc nanoparticles (Zn-NPs) in mitigating abiotic and biotic stress in Pangasius hypophthalmus. Two zinc nanoparticle-incorporated diets with 10 and 20 mg/kg nanoparticles and a control without zinc nanoparticles were formulated. To study the effect of formulated feeds on stress tolerance, fish were exposed to sublethal dose (4 ppm) of Pb (lead) and temperature at 34 °C. Two hundred and seventy-three fish were randomly distributed into seven treatment groups in triplicates, namely a control group (no Zn-NPs and no Pb and temperature exposure, Ctr/Ctr), control diet fed and exposed to Pb (Ctr/Pb), control diet fed and concurrently exposed to Pb and temperature (Pb-T/Ctr), and Zn-NPs 10 and 20 mg/kg diet with or without stressors (Zn-NPs 10 mg/kg, Zn-NPs 20 mg/kg, Pb-T/Zn-NPs 10 mg/kg, Pb-T/Zn-NPs 20 mg/kg). The effect of Zn-NPs on growth performance, stress biomarkers, biochemical and immunological responses, and survival of P. hypophthalmus following challenge with pathogenic bacteria were evaluated. The growth performance was noticeably (p < 0.01) enhanced, and anti-oxidative stress (catalase, superoxide dismutase, and glutathione-s-transferase) significantly reduced in the Zn-NPs supplemented groups. Similarly, immunological parameters such as total protein, albumin, globulin, and A/G ratio significantly improved, and stress biomarkers such as blood glucose, cortisol, and HSP 70 were reduced in Zn-NPs supplemented groups. Overall, the results suggest that supplementation of dietary Zn-NPs with less concentration in the diet has a definitive role in the mitigation of abiotic and biotic stress in P. hypophthalmus.

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.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Sri Sindhura K, Prasad TNVKV, Selvam PP, Hussain OM (2014) Synthesis, characterization and evaluation of effect of phytogenic zinc nanoparticles on soil exo-enzymes. Appl Nanosci 4:819–827. https://doi.org/10.1007/s13204-013-0263-4

    Article  CAS  Google Scholar 

  2. Piccinno F, Gottschalk F, Seeger S, Nowack B (2012) Industrial production quantities and uses of ten engineered nanomaterials for Europe and the world. J Nanopart Res 14:1109–1120. https://doi.org/10.1007/s11051-012-1109-9

    Article  Google Scholar 

  3. Padmavathy N, Vijayaraghavan R (2008) Enhanced bioactivity of ZnO nanoparticles-an antimicrobial study. Sci Technol Adv Mater 9(3):035004

    Article  PubMed  PubMed Central  Google Scholar 

  4. Sahoo A, Swain RK, Mishra SK, Jena B (2014) Serum biochemical indices of broiler birds fed on inorganic, organic and nano zinc supplemented diets. Int J Recent Scientific Res 5:2078–2081

    Google Scholar 

  5. Zhao CY, Tan SX, Xiao XY, Qiu XS, Pan JQ, Tang ZX (2014) Effects of dietary zinc oxide nanoparticles on growth performance and antioxidative status in broilers. Biol Trace Elem Res 160:361–367. https://doi.org/10.1007/s12011-014-0052-2

    Article  CAS  PubMed  Google Scholar 

  6. Wang LZ (2004) Zinc oxide nanostructures: growth, properties and applications. J Phys Condens Matter 16(04):58969–58965. https://doi.org/10.1088/0953-8984/16/25/R01

    Article  CAS  Google Scholar 

  7. Mishra A, Swain RK, Mishra SK, Panda N, Sethy K (2014) Growth performance and serum biochemical parameters as affected by nano zinc supplementation in layer chicks. Indian J Anim Nutr 31:384–388

    Google Scholar 

  8. Swain PS, Somu Rao BNS, Rajendran D, Dominic G, Selvaraju S (2016) Nano zinc, an alternative to conventional zinc as animal feed supplement: a review. Anim Nutr 2:134–141. https://doi.org/10.1016/j.aninu.2016.06.003

    Article  PubMed  PubMed Central  Google Scholar 

  9. Zalewski PD, Ai QT, Dion G, Lata J, Chiara M, Richard ER (2005) Zinc metabolism in airway epithelium and airway inflammation: basic mechanisms and clinical targets: a review. Pharmacol Ther 105:127–149. https://doi.org/10.1016/j.pharmthera.2004.09.004

    Article  CAS  PubMed  Google Scholar 

  10. Prasad AS (1991) Discovery of human zinc deficiency and studies in an experimental human model. Am J Clin Nutr 53:403–412

    Article  CAS  PubMed  Google Scholar 

  11. Wang B, Feng WY, Wang TC, Jia G, Wang M, Shi JW, Zhang F, Zhao YL, Chai ZF (2006) Acute toxicity of nano-and micro-scale zinc powder in healthy adult mice. Toxicol Lett 161:115–123. https://doi.org/10.1016/j.toxlet.2005.08.007

    Article  CAS  PubMed  Google Scholar 

  12. Kumar N, Krishnani KK, Meena KK, Gupta SK, Singh NP (2017) Oxidative and cellular metabolic stress of Oreochromis mossambicus as biomarkers indicators of trace element contaminants. Chemosphere 171:265–274. https://doi.org/10.1016/j.chemosphere.2016.12.066

    Article  CAS  PubMed  Google Scholar 

  13. Kumar N, Krishnani KK, Gupta SK, Singh NP (2017) Cellular stress and histopathological tools used as biomarkers in Oreochromis mossambicus for assessing metal contamination. Environ Toxicol Pharmacol 49:137–147. https://doi.org/10.1016/j.etap.2016.11.017

    Article  CAS  PubMed  Google Scholar 

  14. Kumar N, Krishnani KK, Kumar P, Jha AK, Gupta SK, Singh NP (2017) Dietary zinc promotes immuno-biochemical plasticity and protects fish against multiple stresses. Fish Shellfish Immunol 62:184–194. https://doi.org/10.1016/j.fsi.2017.01.017

    Article  CAS  PubMed  Google Scholar 

  15. Noyes PD, McElwee MK, Miller HD, Clark BW, Van Tiem LA, Walcott KC, Erwin KN, Levin ED (2009) The toxicology of climate change: environmental contaminants in a warming world. Environ Int 35:971–986. https://doi.org/10.1016/j.envint.2009.02.006

    Article  CAS  PubMed  Google Scholar 

  16. IPCC (2007) Intergovernmental panel on climate change, fourth assessment report. Cambridge University Press, New York

    Google Scholar 

  17. Kumar N, Krishnani KK, Chandan NK, Singh NP (2017) Dietary zinc potentiates thermal tolerance and cellular stress protection of Pangasius hypophthalmusreared under lead and thermal stress. Aquac Res 49:1105–1115. https://doi.org/10.1111/are.13560

    Article  CAS  Google Scholar 

  18. Jackson RN, Baird D, Els S (2005) The effect of the heavy metals, lead (Pb 2+) and zinc (Zn 2+) on the brood and larval development of the burrowing crustacean, Callianassa kraussi. Water S A 31(1):107–116

    Article  CAS  Google Scholar 

  19. Rabitto IS, Alves JRMC, Silva de Assis HC, Pelletier EE, Akaishi FM, Anjos A, Randi MF, Ribeiro OCA (2005) Effects of dietary Pb (II) and tributyltin on neotropical fish, Hoplias malabaricus: histopathological and biochemical findings. Ecotoxicol Environ Saf 60:147–156. https://doi.org/10.1016/j.ecoenv.2004.03.002

    Article  CAS  PubMed  Google Scholar 

  20. Yildirim Y, Gonulalan Z, Narin I, Soylak M (2009) Evaluation of trace heavy metal levels of some fish species sold at retail in Kayseri, Turkey. Environ Monit Asses 149:223–228. https://doi.org/10.1007/s10661-008-0196-7

    Article  CAS  Google Scholar 

  21. Hutchins DA, Teyssié JL, Boisson F, Fowler SW, Fisher NS (1996) Temperature effects on uptake and retention of contaminant radionuclides and trace metals by the brittle star Ophiothrix fragilis. Mar Environ Res 41:363–378. https://doi.org/10.1016/0141-1136(95)00026-7

    Article  CAS  Google Scholar 

  22. Heugens EHW, Hendriks AJ, Dekker T, van Straalen NM, Admiraal W (2002) A review of the effects of multiple stressors on aquatic organisms and analysis of uncertainty factors for use in risk assessment. Crit Rev Toxicol 31(3):247–284. https://doi.org/10.1080/20014091111695

    Article  Google Scholar 

  23. Kumar N, Jadhao SB, Chandan NK, Akhlak MD, Rana RS (2012) Methyl donors potentiates growth, metabolic status and neurotransmitter enzyme in Labeo rohita fingerlings exposed to endosulfan and temperature. Fish Physiol Biochem 38(5):1343–1353. https://doi.org/10.1007/s10695-012-9622-4

    Article  CAS  PubMed  Google Scholar 

  24. Kumar N, Minhas PS, Ambasankar K, Krishnani KK, Rana RS (2014) Dietary lecithin potentiates thermal tolerance and cellular stress protection of milk fish (Chanos chanos) reared under low dose endosulfan induced stress. J Therm Biol 46:40–46. https://doi.org/10.1016/j.jtherbio.2014.10.004

    Article  CAS  PubMed  Google Scholar 

  25. Kumar N, Ambasankar K, Krishnani KK, Kumar P, Akhtar MS, Bhushan S, Minhas PS (2016) Dietary pyridoxine potentiates thermal tolerance, heat shock protein and protect against cellular stress of milk fish (Chanos chanos) under endosulfan-induced stress. Fish Shellfish Immunol 55:407–414. https://doi.org/10.1016/j.fsi.2016.06.011

    Article  CAS  PubMed  Google Scholar 

  26. Kumar N, Krishnani KK, Singh NP (2017) Temperature induces lead toxicity in Pangasius hypophthalmus: an acute test, antioxidative status and cellular metabolic stress. Int J Environ Sci Technol 15:57–68. https://doi.org/10.1007/s13762-017-1364-5

    Article  CAS  Google Scholar 

  27. Kumar N, Krishnani KK, Kumar P, Singh NP (2017) Zinc nanoparticles potentiates thermal tolerance and cellular stress protection of Pangasius hypophthalmus reared under multiple stressors. J Therm Biol 70:61–68. https://doi.org/10.1016/j.jtherbio.2017.10.003

    Article  CAS  PubMed  Google Scholar 

  28. Kumar N, Krishnani KK, Singh NP (2018) Comparative study of selenium and selenium nanoparticles with reference to acute toxicity, biochemical attributes and histopathological response in fish. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-017-1165-x

    Article  CAS  PubMed  Google Scholar 

  29. Kumar N, Krishnani KK, Gupta SK, Singh NP (2017) Selenium nanoparticles enhanced thermal tolerance and maintain cellular stress protection of Pangasius hypophthalmus reared under lead and high temperature. Respir Physiol Neurobiol 246:107–116. https://doi.org/10.1016/j.resp.2017.09.006

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  31. Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175

    CAS  PubMed  Google Scholar 

  32. Takahara S, Hamilton BH, Nell JV, Kobra TY, Ogura Y, Nishimura ET (1960) Hypocatalesemia, a new generis carrier state. J Clin Invest 29:610–619. https://doi.org/10.1172/JCI104075

    Article  Google Scholar 

  33. Habing WH, Pabst MN, Bjacoby W (1947) Glutathione S-transferases. Transferase, the first enzymatic step in mercatpopunc acid formation. J Biol Chem 249:7130–7139

    Google Scholar 

  34. Hestrin S (1949) The reaction of acetyl choline and other carboxylic acid derivatives with hydroxylamine and its analytical application. J Biol Chem 180:249–261

    CAS  PubMed  Google Scholar 

  35. Secombes CJ (1990) Isolation of salmonid macrophage and analysis of their killing activity. In: Stolen JSTC, Fletcher DP, Anderson BS, Van Muiswinkel WB (eds) Techniques in fish immunology. SOS publication, fair haven (NJ), pp 137–152

    Google Scholar 

  36. Stasiack AS, Bauman CP (1996) Neutrophil activity as a potent indicator concomitant analysis. Fish Shellfish Immunol 37:539

    Google Scholar 

  37. Doumas BT, Watson W, Biggs HG (1971) Albumin standards and measurement of serum albumin with bromocresol green. Clin Chim Acta 31:87–96. https://doi.org/10.1016/0009-8981(71)90365-2

    Article  CAS  PubMed  Google Scholar 

  38. Nelson N (1944) A photometric adaptation of the Somogyi method for the determination of glucose. J Biol Chem 153:375–380

    CAS  Google Scholar 

  39. Somoyogi M (1945) A new reagent for the determination of sugars. J Biol Chem 160:61–68

    Google Scholar 

  40. Muralisankar T, Bhavan PS, Radhakrishnan S, Seenivasan C, Manickam N, Srinivasan V (2014) Dietary supplementation of zinc nanoparticles and its influence on biology, physiology and immune responses of the freshwater prawn, Macrobrachium rosenbergii. Biol Trace Elem Res 160:56–66. https://doi.org/10.1007/s12011-014-0026-4

    Article  CAS  PubMed  Google Scholar 

  41. Petrovic V, Nollet L, Kovac G (2010) Effect of dietary supplementation of trace elements on the growth performance and their distribution in the breast and thigh muscles depending on the age of broiler chickens. Acta Vet Brno 79:203–209. https://doi.org/10.2754/avb201079020203

    Article  CAS  Google Scholar 

  42. Hao L, Chen L, Hao J, Zhong N (2013) Bioaccumulation and sub-acute toxicity of zinc oxide nanoparticles in juvenile carp (Cyprinus carpio): a comparative study with its bulk counterparts. Ecotoxicol Environ Saf 91:52–60. https://doi.org/10.1016/j.ecoenv.2013.01.007

    Article  CAS  PubMed  Google Scholar 

  43. Alishahi A, Mirvaghefi A, Tehrani MR, Farahmand FA, Shojaosadati SA, Dorkoosh FA (2011) Shelf life and delivery enhancement of vitamin C using chitosan nanoparticles. Food Chem 126:935–940. https://doi.org/10.1016/j.foodchem.2010.11.086

    Article  CAS  Google Scholar 

  44. Imamoglu S, Bereket A, Turan S, Tagaand Y, Haklar G (2005) Effect of zinc supplementation on growth hormone secretion, IGF-I, IGFBP-3,somatomedin generation, alkaline phosphatase, osteocalcin and growth in prepubertal children with idiopathic short stature. J Pediatr Endocrinol Metab 18:69–74. https://doi.org/10.1515/JPEM.2005.18.1.69

    Article  CAS  PubMed  Google Scholar 

  45. Siklar Z, Tuna C, Dallar Y, Tanyer G (2003) Zinc deficiency: a contributing factor of short stature in growth hormone deficient children. J Trop Pediatr 49:187–188

    Article  PubMed  Google Scholar 

  46. Kumar N, Gupta S, Chandan NK, Aklakur M, Pal AK, Jadhao SB (2014) Lipotropes protect against pathogen-aggravated stress and mortality in low dose pesticide-exposed fish. PLoS One 9(4):e93499. https://doi.org/10.1371/journal.pone.0093499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Kumar N, Ambasankar K, Krishnani KK, Bhushan S, Minhas PS (2016) Dietary pyridoxine protects against stress and maintains immune-hematological status in Chanos Chanos exposed to endosulfan. Basic Clin Pharmacol Toxicol 119:297–308. https://doi.org/10.1111/bcpt.12589

    Article  CAS  PubMed  Google Scholar 

  48. Dhawan DK, Chadha VD (2010) Zinc: a promising agent in dietary chemoprevention of cancer. Indian J Med Res 132:676–682

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Verstraeten SV, Zago MP, MacKenzie GG, Keen CL, Oteiza PI (2004) Influence of zinc deficiency on cell-membrane fluidity in Jurkat, 3T3 and IMR-32 cells. Biochem J 378:579–587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Tapiero H, Tew KD (2003) Trace elements in human physiology and pathology: zinc and metallothioneins. Biomed Pharmacother 57:399–411. https://doi.org/10.1016/S0753-3322(03)00081-7

    Article  CAS  PubMed  Google Scholar 

  51. Muthappa NA, Gupta S, Yengkokpam S, Debnath D, Kumar N, Pal AK, Jadhao SB (2014) Lipotropes promote immunobiochemical plasticity and protect fish against low-dose pesticide-induced oxidative stress. Cell Stress Chaperons 19(1):61–81. https://doi.org/10.1007/s12192-013-0434-y

    Article  CAS  Google Scholar 

  52. Murphy SD (1986) Pesticides. The basic science of poisons. Macmillan, New York, pp 519–581

    Google Scholar 

  53. Miranda RR, Damaso da Silveira AL, de Jesus IP, Grotzner SR, Voigt CL, Campos SX, Garcia JR, Randi MA, Ribeiro CA, Filipak Neto F (2016) Effects of realistic concentrations of TiO2 and ZnO nanoparticles in Prochilodus lineatus juvenile fish. Environ Sci Pollut Res 23(6):5179–5188. https://doi.org/10.1007/s11356-015-5732-8

    Article  CAS  Google Scholar 

  54. Colovic MB, Krstic DZ, Lazarevic-Pasti TD, Bondzic AM, Vasic VM (2013) Acetylcholinesterase inhibitors. Curr Neuropharmacol 11(3):315–335. https://doi.org/10.2174/1570159X11311030006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Espanani HR, Kobra S, Leila S, Vahid YB, Esmaiel A (2014) Investigation of the zinc oxide nanoparticles effect on testosterone, cholesterol and cortisol in rats. Res J Recent Sci 3(4):14–19

    Google Scholar 

  56. Yousefi Babadi V, Amraeai E, Salehh H, Sadeghi L, Najafi L, Fazilati M (2013) Evaluation of iron oxide nanoparticles effects on tissue and enzymes of thyroid in rats. Int Res J Biological Sci 2:67–69

    Google Scholar 

  57. Morimoto RI (1993) Cells in stress: transcriptional activation of heat shock genes. Science 259:1409–1410

    Article  CAS  PubMed  Google Scholar 

  58. Chowdhury MJ, Pane EF, Wood CM (2004) Physiological effects of dietary cadmium acclimation and waterborne cadmium challenge in rainbow trout: respiratory, ionoregulatory, and stress parameters. Comp Biochem Physiol C: Toxicol Pharmacol 139:163–173. https://doi.org/10.1016/j.cca.2004.10.006

    Article  CAS  Google Scholar 

  59. Jiang D, Wu Y, Huang D, Ren X, Wang Y (2017) Effect of blood glucose level on acute stress response of grass carp Ctenopharyngodon idella. Fish Physiol Biochem 43:1433–1442. https://doi.org/10.1007/s10695-017-0383-y

    Article  CAS  PubMed  Google Scholar 

  60. Pottinger TG (1998) Changes in blood cortisol, glucose and lactate in carp retained in anglers’ keepnets. J Fish Biol 53:728–742. https://doi.org/10.1111/j.1095-8649.1998.tb01828.x

    Article  CAS  Google Scholar 

  61. Haase H, Maret W (2005) Protein tyrosine phosphatases as targets of the combined insulinomimetic effects of zinc and oxidants. Biometals 18:333–338. https://doi.org/10.1007/s10534-005-3707-9

    Article  CAS  PubMed  Google Scholar 

  62. Tang X, Shay NF (2001) Zinc has an insulin-like effect on glucose transport mediated by phosphoinositol-3-kinase and Akt in 3T3-L1 fibroblasts and adipocytes. J Nutr 131:1414–1420

    Article  CAS  PubMed  Google Scholar 

  63. Wijesekara N, Chimienti F, Wheeler MB (2009) Zinc, a regulator of islet function and glucose homeostasis. Diabetes Obes Metab 11(Suppl 4):202–214. https://doi.org/10.1111/j.1463-1326.2009.01110.x

    Article  CAS  PubMed  Google Scholar 

  64. Valencia PM, Farokhzad OC, Karnik R, Langer R (2012) Microfluidic technologies for accelerating the clinical translation of nanoparticles. Nat Nanotechnol 7:623–629. https://doi.org/10.1038/nnano.2012.168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Espitia P, Soares ND, Coimbra JD, de Andrade N, Cruz R, Medeiros E (2012) Zinc oxide nanoparticles: synthesis, antimicrobial activity and food packaging applications. Food Bioprocess Technol 5:1447–1464. https://doi.org/10.1007/s11947-012-0797-6

    Article  CAS  Google Scholar 

  66. Sarwar S, Chakraborti S, Bera S, Sheikh IA, Hoque KM, Chakrabarti P (2016) The antimicrobial activity of ZnO nanoparticles against Vibrio cholerae: variation in response depends on biotype. Nanomedicine 12:1499–1509. https://doi.org/10.1016/j.nano.2016.02.006

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors express sincere gratitude to the Director, ICAR-National Institute of Abiotic Stress Management, Baramati, Pune, for providing all the facilities to conduct the present work. The financial assistance has been provided by Indian Council of Agricultural Research (ICAR), New Delhi, India, as an institutional project (no. IXX09673) is gratefully acknowledged. Authors are grateful to Dr. Veera M. Boddu, Research Leader, National Centre for Agriculture Utilization Research (NCAUR) Agricultural Research Service, US Department of Agriculture, ARS/USDA USA, Dr. Sanath H Kumar, Senior Scientist, Central Institute of Fisheries Education, Mumbai India, and Dr. Sib Sankar Giri, Laboratory of Aquatic Biomedicine, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul, South Korea, for English editing and correction. I also place a record of thanks to Mrs. Yogita and Mr. Yuvraj Sanas for their technical assistance.

Author information

Authors and Affiliations

  1. ICAR-National Institute of Abiotic Stress Management (NIASM), Malegaon, Pune, Baramati, 413115, India

    Neeraj Kumar, Kishore Kumar Krishnani & Narendra Pratap Singh

Authors
  1. Neeraj Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kishore Kumar Krishnani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Narendra Pratap Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Neeraj Kumar.

Ethics declarations

Conflict of Interest

All authors declare that they have no conflict of interest.

Electronic Supplementary Material

ESM 1

(DOCX 847 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kumar, N., Krishnani, K.K. & Singh, N.P. Effect of Dietary Zinc-Nanoparticles on Growth Performance, Anti-Oxidative and Immunological Status of Fish Reared Under Multiple Stressors. Biol Trace Elem Res 186, 267–278 (2018). https://doi.org/10.1007/s12011-018-1285-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-018-1285-2

Keywords

Search

Navigation