Skip to main content

Advertisement

SpringerLink
Log in

Zinc Oxide Nanoparticles Significant Role in Poultry and Novel Toxicological Mechanisms

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

Abstract

Zinc oxide nanoparticles (ZnO NPs) have involved a lot of consideration owing to their distinctive features. The ZnO NPs can be described as particularly synthesized mineral salts via nanotechnology, varying in size from 1 to 100 nm, while zinc oxide (ZnO), it is an inorganic substrate of zinc (Zn). The Zn is a critical trace element necessary for various biological and physiological processes in the body. Studies have revealed ZnO NPs’ efficient immuno-modulatory, growth-promoting, and antimicrobial properties in poultry birds. They offer increased bioavailability as compared to their traditional sources, producing better results in terms of productivity and welfare and consequently reducing ecological harm in the poultry sector. However, they have also been reported for their toxicological effects, which are size, shape, concentration, and exposure route dependent. The investigations done so far have yielded inconsistent results, therefore, a lot of additional studies and research are required to clarify the harmful consequences of ZnO NPs and to bring them to a logical end. This review explores an overview of efficient possible role of ZnO NPs, while comparing them with other nutritional Zn sources, in the poultry industry, primarily as dietary supplements that effect the growth, health, and performance of the birds. In addition to the anti-bacterial mechanisms of ZnO NPs and their promising role as antifungal, and anti-colloidal agent, this paper also covers the toxicological mechanisms of ZnO NPs and their consequent toxicological hazards to vital organs and the reproductive system of poultry birds.

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

Data Availability

All data are available with us and will submit once a reasonable request needed.

References

  1. Abass MA, Selim SA, Selim AO, El-Shal AS, Gouda ZA (2017) Effect of orally administered zinc oxide nanoparticles on albino rat thymus and spleen. IUBMB Life 69(7):528–539

    Article  CAS  PubMed  Google Scholar 

  2. Abd El-Hack ME, Alaidaroos BA, Farsi RM, Abou-Kassem DE, El-Saadony MT, Saad AM, ... Ashour EA (2021) Impacts of supplementing broiler diets with biological curcumin, zinc nanoparticles and Bacillus licheniformis on growth, carcass traits, blood indices, meat quality and cecal microbial load. Animals 11(7):1878

  3. Abdel-Halim KY, Osman SR, Abdou GY (2020) In vivo evaluation of oxidative stress and biochemical alteration as biomarkers in glass clover snail, Monacha cartusiana exposed to zinc oxide nanoparticles. Environ Pollut 257:113120

    Article  CAS  PubMed  Google Scholar 

  4. Abedini M, Shariatmadari F, Torshizi MK, Ahmadi H (2017) Effects of a dietary supplementation with zinc oxide nanoparticles, compared to zinc oxide and zinc methionine, on performance, egg quality, and zinc status of laying hens. Livest Sci 203:30–36

    Article  Google Scholar 

  5. Abedini M, Shariatmadari F, Karimi Torshizi MA, Ahmadi H (2018) Effects of zinc oxide nanoparticles on the egg quality, immune response, zinc retention, and blood parameters of laying hens in the late phase of production. J Anim Physiol Anim Nutr (berl) 102(3):736–745

    Article  CAS  PubMed  Google Scholar 

  6. Abercrombie M, Ambrose EJ (1962) The surface properties of cancer cells: a review. Cancer Res 22:525–548

    CAS  PubMed  Google Scholar 

  7. Abo-Al-Ela HG, El-Kassas S, El-Naggar K, Abdo SE, Jahejo AR, Al Wakeel RA (2021) Stress and immunity in poultry: light management and nanotechnology as effective immune enhancers to fight stress. Cell Stress Chaperones 26:457–472

    Article  PubMed  PubMed Central  Google Scholar 

  8. Agarwal H, Menon S, Kumar SV, Rajeshkumar S (2018) Mechanistic study on antibacterial action of zinc oxide nanoparticles synthesized using green route. Chem Biol Interact 286:60–70

    Article  CAS  Google Scholar 

  9. Ahmadi F, Ebrahimnezjad Y, Ghalehkandi JG, Sis NM (2014) The effect of dietary zinc oxide nanoparticles on the antioxidant state and serum enzymes activity in broiler chickens during starter stage. In: International Conference on Biological, Civil and Environmental Engineering. Dubai, pp 26–28

  10. Ahmadi F, Ebrahimnezhad Y, Sis NM, Ghiasi J (2013) The effects of zinc oxide nanoparticles on performance, digestive organs and serum lipid concentrations in broiler chickens during starter period. Int J Biosci 3(7):23–29

    Article  Google Scholar 

  11. Aijie C, Huimin L, Jia L, Lingling O, Limin W, Junrong W, Xuan L, Xue H, Longquan S (2017) Central neurotoxicity induced by the instillation of ZnO and TiO2 nanoparticles through the taste nerve pathway. Nanomedicine 12:2453–2470

    Article  PubMed  Google Scholar 

  12. Akhavan-Salamat H, Ghasemi HA (2019) Effect of different sources and contents of zinc on growth performance, carcass characteristics, humoral immunity and antioxidant status of broiler chickens exposed to high environmental temperatures. Livest Sci 223:76–83

    Article  Google Scholar 

  13. Akhtar MJ, Ahamed M, Kumar S, Khan MM, Ahmad J, Alrokayan SA (2012) Zinc oxide nanoparticles selectively induce apoptosis in human cancer cells through reactive oxygen species. Int J Nanomedicine 7:845–857

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Ali MZ, Sana S, Sheikh AA, Maheen Z (2022) Molecular characterization of toxigenic Aspergillus flavus isolated from sick broiler lungs and risk factors analysis. Pak Vet J 42(2):194–200. https://doi.org/10.29261/pakvetj/2022.037

  15. Ali S, Masood S, Zaneb H, Faseeth-ur-Rehman H, Masood S, Khan M, Tahir SK, Rehman H (2017) Supplementation of zinc oxide nanoparticles has beneficial effects on intestinal morphology in broiler chicken. Pak Vet J 37:335–339

    CAS  Google Scholar 

  16. Ali A, Phull AR, Zia M (2018) Elemental zinc to zinc nanoparticles: Is ZnO NPs crucial for life? Synthesis, toxicological, and environmental concerns. Nanotechnol Rev 7(5):413–441

    Article  CAS  Google Scholar 

  17. Alkhtib A, Scholey D, Carter N, Cave GW, Hanafy BI, Kempster SR, Mekapothula S, Roxborough ET, Burton EJ (2020) Bioavailability of methionine-coated zinc nanoparticles as a dietary supplement leads to improved performance and bone strength in broiler chicken production. Animals 10:1482

    Article  PubMed  PubMed Central  Google Scholar 

  18. Almansour MI, Alferah MA, Shraideh ZA, Jarrar BM (2017) Zinc oxide nanoparticles hepatotoxicity: histological and histochemical study. Environ Toxicol Pharmacol 51:124–130

    Article  CAS  PubMed  Google Scholar 

  19. Altaf S, Umair M (2022) Green nanotechnology mediated silver and iron oxide nanoparticles: Potential antimicrobials. Agrobiol Rec 10:26–31

    Google Scholar 

  20. Ao T, Pierce J (2013) The replacement of inorganic mineral salts with mineral proteinates in poultry diets. Worlds Poult Sci J 69(1):5–16

    Article  Google Scholar 

  21. Arabi F, Imandar M, Negahdary M, Imandar M, Noughabi MT, Akbari-dastjerdi H, Fazilati M (2012) Investigation anti-bacterial effect of zinc oxide nanoparticles upon life of Listeria monocytogenes. Ann Biol Res 7:3679–3685

    Google Scholar 

  22. Asheer M, Manwar SJ, Gole MA, Sirsat S, Wade MR, Khose KK, Ali SS (2018) Effect of dietary nano zinc oxide supplementation on performance and zinc bioavailability in broilers. 53(1):70–75

  23. Attia H, Nounou H, Shalaby M (2018) Zinc oxide nanoparticles induced oxidative DNA damage, inflammation and apoptosis in rat’s brain after oral exposure. Toxics 6:29

    Article  PubMed  PubMed Central  Google Scholar 

  24. Auffan M, Rose J, Bottero JY, Lowry GV, Jolivet JP, Wiesner MR (2009) Towards a definition of inorganic nanoparticles from an environmental, health and safety perspective. Nat Nanotechnol 4:634–641

    Article  CAS  PubMed  Google Scholar 

  25. Ayala A, Muñoz MF, Argüelles S (2014) Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid Med Cell Longev 2014:1–31

    Article  CAS  Google Scholar 

  26. Bakr AF, Abdelgayed SS, EL-Tawil OS, Bakeer AM (2020) Ginger extract and ginger nanoparticles; characterization and applications. Int J Vet Sci 9:203–209

    Google Scholar 

  27. Bao YM, Choct M (2009) Trace mineral nutrition for broiler chickens and prospects of application of organically complexed trace minerals: a review. Anim Prod Sci 49:269–282

    Article  CAS  Google Scholar 

  28. Barkhordari A, Hekmatimoghaddam S, Jebali A, Khalili MA, Talebi A, Noorani M (2013) Effect of zinc oxide nanoparticles on viability of human spermatozoa. Iran J Appl Anim Sci 11(9):767

    CAS  Google Scholar 

  29. Batool S, Munir F, Sindhu ZuD, Abbas RZ, Aslam B, Khan MK, Imran M, Aslam MA, Ahmad M, Chaudhary MK (2023) In vitro anthelmintic activity of Azadirachta indica (neem) and Melia azedarach (bakain) essential oils and their silver nanoparticles against Haemonchus contortus. Agrobiol Rec 11:6–12

    Article  Google Scholar 

  30. Bhattacharya D, Santra CR, Ghosh AN, Karmakar P (2014) Differential toxicity of rod and spherical zinc oxide nanoparticles on human peripheral blood mononuclear cells. J Biomed Nanotechnol 10(4):707–716

    Article  CAS  PubMed  Google Scholar 

  31. Bisht G, Rayamajhi S (2016) ZnO nanoparticles: a promising anticancer agent. Nanobiomedicine 3(Godište 2016):3–9

  32. Biswas SK (2016) Does the interdependence between oxidative stress and inflammation explain the antioxidant paradox? Oxid Med Cell Longev 2016:1–9

    Article  Google Scholar 

  33. Bonaventura P, Benedetti G, Albarède F, Miossec P (2015) Zinc and its role in immunity and inflammation. Autoimmun Rev 14:277–285

    Article  CAS  PubMed  Google Scholar 

  34. Bondarenko O, Juganson K, Ivask A, Kasemets K, Mortimer M, Kahru A (2013) Toxicity of Ag, CuO and ZnO nanoparticles to selected environmentally relevant test organisms and mammalian cells in vitro: a critical review. Arch Toxicol 87:1181–1200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Boroumand Moghaddam A, Moniri M, Azizi S, Abdul RR, Bin AA, Zuhainis SW, Namvar F, Navaderi M, Mohamad R (2017) Biosynthesis of ZnO nanoparticles by a new Pichia kudriavzevii yeast strain and evaluation of their antimicrobial and antioxidant activities. Molecules 22:872

    Article  PubMed Central  Google Scholar 

  36. Bratz K, Gölz G, Riedel C, Janczyk P, Nöckler K, Alter T (2013) Inhibitory effect of high-dosage zinc oxide dietary supplementation on Campylobacter coli excretion in weaned piglets. J Appl Microbiol 115:1194–1202

    Article  CAS  PubMed  Google Scholar 

  37. Brun NR, Lenz M, Wehrli B, Fent K (2014) Comparative effects of zinc oxide nanoparticles and dissolved zinc on zebrafish embryos and eleuthero-embryos: importance of zinc ions. Sci Total Environ 476:657–666

    Article  PubMed  Google Scholar 

  38. Burns AA, Vider J, Ow H, Herz E, Penate-Medina O, Baumgart M, Larson SM, Wiesner U, Bradbury M (2009) Fluorescent silica nanoparticles with efficient urinary excretion for nanomedicine. Nano Lett 9:442–448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Byrne CS, Chambers ES, Morrison DJ, Frost G (2015) The role of short chain fatty acids in appetite regulation and energy homeostasis. Int J Obes 39:1331–1338

    Article  CAS  Google Scholar 

  40. Cadet J, Douki T, Gasparutto D, Ravanat JL (2003) Oxidative damage to DNA: formation, measurement and biochemical features. Mutat Res 531:5–23

    Article  CAS  PubMed  Google Scholar 

  41. Chakraborti S, Chatterjee T, Joshi P, Poddar A, Bhattacharyya B, Singh SP, Gupta V, Chakrabarti P (2010) Structure and activity of lysozyme on binding to ZnO nanoparticles. Langmuir 26:3506–3513

    Article  CAS  PubMed  Google Scholar 

  42. Chang YN, Zhang M, Xia L, Zhang J, Xing G (2012) The toxic effects and mechanisms of CuO and ZnO nanoparticles. Materials 5:2850–2871

    Article  CAS  PubMed Central  Google Scholar 

  43. Chang YT, Chang WN, Tsai NW, Huang CC, Kung CT, Su YJ, Lin WC, Cheng BC, Su CM, Chiang YF, Lu CH (2014) The roles of biomarkers of oxidative stress and antioxidant in Alzheimer’s disease: a systematic review. Biomed Res Int 2014:1–14

    Google Scholar 

  44. Chen TH, Lin CC, Meng PJ (2014) Zinc oxide nanoparticles alter hatching and larval locomotor activity in zebrafish (Danio rerio). J Hazard Mater 277:134–140

    Article  CAS  PubMed  Google Scholar 

  45. Chia SL, Leong DT (2016) Reducing ZnO nanoparticles toxicity through silica coating. Heliyon 2(10): e00177

  46. Cho WS, Kang BC, Lee JK, Jeong J, Che JH, Seok SH (2013) Comparative absorption, distribution, and excretion of titanium dioxide and zinc oxide nanoparticles after repeated oral administration. Part Fibre Toxicol 10:1–9

    Article  Google Scholar 

  47. Chong CL, Fang CM, Pung SY, Ong CE, Pung YF, Kong C, Pan Y (2021) Current updates on the in vivo assessment of zinc oxide nanoparticles toxicity using animal models. BioNanoScience 11:590–620

    Article  Google Scholar 

  48. Christianson DW (1991) Structural biology of zinc. Adv Protein Chem 42:281–355

    Article  CAS  PubMed  Google Scholar 

  49. Classen HG, Gröber U, Löw D, Schmidt J, Stracke H (2011) Zinc deficiency. Symptoms, cuses, diagnosis and therapy. Med Monatsschr Pharm 34:87–95

    CAS  PubMed  Google Scholar 

  50. Council NR (1994) Nutrient Requirements of Poultry. 9th edWashington, DC: Natl

  51. Davis ME, Chen Z, Shin DM (2008) Nanoparticle therapeutics: an emerging treatment modality for cancer. Nat Rev Drug Discov 7(9):771–782

    Article  CAS  PubMed  Google Scholar 

  52. De Andrade Vieira JE, de Oliveira Ferreira R, dos Reis Sampaio DM, da Costa AAP, Malafaia G (2019) An in-sight on the mutagenicity and cytotoxicity of zinc oxide nano-particles in Gallus gallus domesticus (Phasianidae). Chemos-Phere 231:10–19

    Article  Google Scholar 

  53. Degen A, Kosec M (2000) Effect of pH and impurities on the surface charge of zinc oxide in aqueous solution. J Eur Ceram Soc 20(6):667–673

    Article  CAS  Google Scholar 

  54. De Grande A, Leleu S, Delezie E, Rapp C, De Smet S, Goossens E, Haesebrouck F, Van Immerseel F, Ducatelle R (2020) Dietary zinc source impacts intestinal morphology and oxidative stress in young broilers. Poult Sci 99:441–453

    Article  PubMed  Google Scholar 

  55. Deng X, Luan Q, Chen W, Wang Y, Wu M, Zhang H, Jiao Z (2009) Nanosized zinc oxide particles induce neural stem cell apoptosis. Nanotechnology 20:115101

    Article  PubMed  Google Scholar 

  56. Dkhil MA, Al-Quraishy S, Wahab R (2015) Anticoccidial and antioxidant activities of zinc oxide nanoparticles on Eimeria papillata-induced infection in the jejunum. Int J Nanomedicine 10:1961–1968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Dukare S, Mir NA, Mandal AB, Dev K, Begum J, Rokade J J, ... Bhanja SK (2021) A comparative study on the antioxidant status, meat quality, and mineral deposition in broiler chicken fed dietary nano zinc viz-a-viz inorganic zinc. J Food Sci Technol 58:834–843

  58. Duzguner V, Kaya S (2007) Effect of zinc on the lipid peroxidation and the antioxidant defense systems of the alloxan-induced diabetic rabbits. Free Radic Biol Med 42:1481–1486

    Article  CAS  PubMed  Google Scholar 

  59. El-Bahr SM, Shousha S, Albokhadaim I, Shehab A, Khattab W, Ahmed-Farid O, El-Garhy O, Abdelgawad AM, El-Naggar M, Moustafa M, Omnia Badr, Shathele M (2020) Impact of dietary zinc oxide nanoparticles on selected serum biomarkers, lipid peroxidation and tissue gene expression of antioxidant enzymes and cytokines in Japanese quail. BMC Vet Res 16(1):1–12

    Article  Google Scholar 

  60. Elbehary M, Dowidar YA, Ashour AM, Abd El Fattah EM, Monir A (2023) Effect of in vitro maturation medium supplementation with chitosan nanoparticles on the River buffalo cumulus-oocyte complexes. Int J Vet Sci 12(3):341–346

    Google Scholar 

  61. El-Dawy K, Saad S, Hussein MMA, Yahia R, Al-Gamal M (2023) Naturally based nano formulation in metabolic and reproductive disorders: A review. Int J Vet Sci 12(1):7–17

    Google Scholar 

  62. El-Hamaky AMA, Hassan AA, Wahba AKA, El Mosalamy MMEA (2023) Influence of copper and zinc nanoparticles on genotyping characterizations of multi-drug resistance genes for some calf pathogens. Int J Vet Sci 12(3):309–317

    Google Scholar 

  63. El-Katcha M, Soltan MA, El-Badry M (2017) Effect of dietary replacement of inorganic zinc by organic or nanoparticles sources on growth performance, immune response and intestinal histopathology of broiler chicken. Alex J Vet Sci 55(2):129–145

    Google Scholar 

  64. El-Sawy AESF, El-Maddawy ZK, Awad AA, Mashalla AW (2021) The growth promoting and immuno-stimulant effects of nano zinc oxide of broiler chicks. Alex J Vet Sci 69(2):16–28

    Google Scholar 

  65. Emmanuel DC, Oyeagu CE, Ogwuegbu MC, Ozochi CU, Ezema C, Akuru AE, Lewu FB (2022) Egg lipid profile, growth traits, blood biomarkers and physical egg characteristics of heavy Ecotype laying hens fed Oregano (Origanum vulgare) meals. Int J Vet Sci 11(3):344–352

    Google Scholar 

  66. Eskandani M, Janmohammadi H, Mirghelenj SA, Ebrahimi M, Kalanaky S (2021) Effects of zinc nanoparticles on growth performance, carcass characteristics, immunity, and meat quality of broiler chickens. Iran J Appl Anim Sci 11(1):135–146

    CAS  Google Scholar 

  67. Fang YZ, Yang S, Wu G (2002) Free radicals, antioxidants, and nutrition. Nutrition 18(10):872–879

    Article  CAS  PubMed  Google Scholar 

  68. Fathi M, Haydari M, Tanha T (2016) Effects of zinc oxide nanoparticles on antioxidant status, serum enzymes activities, biochemical parameters and performance in broiler chickens. J Livest Sci Technol 4:7–13

    Google Scholar 

  69. FDA U (2015) Select committee on GRAS substances (SCOGS) opinion: tannic acid (hydrolyzable gallotannins). GRAS Substances (SCOGS) Database 4:203–211

  70. Feng Y, Gong J, Yu H, Jin Y, Zhu J, Han Y (2010) Identification of changes in the composition of ileal bacterial microbiota of broiler chickens infected with Clostridium perfringens. Vet Microbiol 140:116–121

    Article  CAS  PubMed  Google Scholar 

  71. Feng JWQM, Ma WQ, Niu HH, Wu XM, Wang Y (2010) Effects of zinc glycine chelate on growth, hematological, and immunological characteristics in broilers. Biol Trace Elem Res 133:203–211

    Article  CAS  PubMed  Google Scholar 

  72. Feng Y, Min L, Zhang W, Liu J, Hou Z, Chu M, Chu M, Li L, Shen W, Zhao Y, Zhang H (2017) Zinc oxide nanoparticles influence microflora in ileal digesta and correlate well with blood metabolites. Front Microbiol 8:992

    Article  PubMed  PubMed Central  Google Scholar 

  73. Fuchs P, Perez-Pinzon MA, Dave KR (2014) Cerebral ischemia in diabetics and oxidative stress. In: Diabetes: Oxidative Stress and Dietary Antioxidants. Academic Press, pp 15–23

  74. Ganapathy K, Ball C, Kabiraj CK, Nooruzzaman M, Chowdhury EH, Islam MR (2021) Mycoplasma gallisepticum detection in Bangladesh table egg laying chicken flocks. Pak Vet J 41(2):306–308. https://doi.org/10.29261/pakvetj/2021.024

  75. Gangadoo S, Stanley D, Hughes RJ, Moore RJ, Chapman J (2016) Nanoparticles in feed: progress and prospects in poultry research. Trends Food Sci Technol 58:115–126

    Article  CAS  Google Scholar 

  76. González SE, Bolaina-Lorenzo E, Pérez-Trujillo JJ, Puente-Urbina BA, Rodríguez-Fernández O, Fonseca-García A, Betancourt-Galindo R (2021) Antibacterial and anticancer activity of ZnO with different morphologies: a comparative study. 3 Biotech 11:1–12

  77. Gopi M, Pearlin B, Kumar RD, Shanmathy M, Prabakar G (2017) Role of nanoparticles in animal and poultry nutrition: modes of action and applications in formulating feed additives and food processing. Int J Pharmacol 13(7):724–31

    Article  CAS  Google Scholar 

  78. Guo D, Wu C, Jiang H, Li Q, Wang X, Chen B (2008) Synergistic cytotoxic effect of different sized ZnO nanoparticles and daunorubicin against leukemia cancer cells under UV irradiation. J Photochem Photobiol B 93:119–126

    Article  CAS  PubMed  Google Scholar 

  79. Hammond B, Hess ML (1985) The oxygen free radical system: potential mediator of myocardial injury. J Am Coll Cardiol 6:215–220

    Article  CAS  PubMed  Google Scholar 

  80. Handa N, Bhardwaj R, Kaur H, Poonam, Kapoor D, Rattan A, Kaur S, Thukral AK, Kaur S, Arora S, Kapoor N (2016) Selenium: an antioxidative protectant in plants under stress. In: Plant metal interaction. Elsevier, pp 179–207

  81. Hanley C, Layne J, Punnoose A, Reddy K, Coombs I, Coombs A, ... Wingett D (2008) Preferential killing of cancer cells and activated human T cells using ZnO nanoparticles. Nanotechnology 19(29):295103

  82. Hong JS, Park MK, Kim MS, Lim JH, Park GJ, Maeng EH, Shin JH, Kim MK, Jeong J, Park JA, Kim JC, Shin HC (2014) Prenatal development toxicity study of zinc oxide nanoparticles in rats. Int J Nanomedicine 9:159

    PubMed  PubMed Central  Google Scholar 

  83. Hong JS, Park MK, Kim MS, Lim JH, Park GJ, Maeng EH, Shin JH, Kim YR, Kim MK, Lee JK, Park JA, Kim JC, Shin HC (2014) Effect of zinc oxide nanoparticles on dams and embryo–fetal development in rats. Int J Nanomedicine 9:145

    PubMed  PubMed Central  Google Scholar 

  84. Huang K, Ma H, Liu J, Huo S, Kumar A, Wei T, ... Liang XJ (2012) Size-dependent localization and penetration of ultrasmall gold nanoparticles in cancer cells, multicellular spheroids, and tumors in vivo. ACS Nano 6(5):4483–4493

  85. Hussain A, Oves M, Alajmi MF, Hussain I, Amir S, Ahmed J, ... Ali I (2019) Biogenesis of ZnO nanoparticles using Pandanus odorifer leaf extract: anticancer and antimicrobial activities. RSC Adv 9(27):15357–15369

  86. Ibrahim D, Ali HA, El-Mandrawy SA (2017) Effects of different zinc sources on performance, bio distribution of minerals and expression of genes related to metabolism of broiler chickens. Zagazig Vet J 45(3):292–304

    Article  Google Scholar 

  87. Ighodaro OM, Akinloye OA (2018) First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid. Alexandria Med J 54:287–293

    Article  Google Scholar 

  88. Imran M, Cao S, Wan SF, Chen Z, Saleemi MK, Wang N, Naseem MN, Munawar J (2020) Mycotoxins—a global one health concern: A review. Agrobiol Rec 2:1–16

    Article  Google Scholar 

  89. Islam MO, Bacchetti T, Ferretti G (2019) Alterations of antioxidant enzymes and biomarkers of nitro-oxidative stress in tissues of bladder cancer. Oxid Med Cell Longev 2019:1–10

    Article  Google Scholar 

  90. Jamdagni P, Khatri P, Rana JS (2018) Green synthesis of zinc oxide nanoparticles using flower extract of Nyctanthes arbor-tristis and their antifungal activity. J King Saud Univ Sci 30:168–175

    Article  Google Scholar 

  91. Jayaseelan C, Rahuman AA, Kirthi AV, Marimuthu S, Santhoshkumar T, Bagavan A, Gaurav K, Karthik L, Rao KB (2012) Novel microbial route to synthesize ZnO nanoparticles using Aeromonas hydrophila and their activity against pathogenic bacteria and fungi. Spectrochim Acta A Mol Biomol Spectrosc 90:78–84

    Article  CAS  PubMed  Google Scholar 

  92. Jeeva JS, Sunitha J, Ananthalakshmi R, Rajkumari S, Ramesh M, Krishnan R (2015) Enzymatic antioxidants and its role in oral diseases. J Pharm Bioallied Sci 7(Suppl 2):S331–S333

    PubMed  PubMed Central  Google Scholar 

  93. Jiang Z, Lin Y, Zhou G, Luo L, Jiang S, Chen F (2009) Effects of dietary selenomethionine supplementation on growth performance, meat quality and antioxidant property in yellow broilers. J Agric Food Chem 57:9769–9772

    Article  CAS  PubMed  Google Scholar 

  94. Jiang SM, Jia L, Zhang MH (2015) Probiotic and lactulose: influence on gastrointestinal flora and pH value in minimal hepatic encephalopathy rats. Int J Clin Exp Med 8:9996

    PubMed  PubMed Central  Google Scholar 

  95. Jiang J, Pi J, Cai J (2018) The advancing of zinc oxide nanoparticles for biomedical applications. Bioinorg Chem Appl 2018:1–18

    Article  Google Scholar 

  96. Jiao J, Wu J, Zhou C, Tang S, Wang M, Tan Z (2016) Composition of ileal bacterial community in grazing goats varies across non-rumination, transition and rumination stages of life. Front Microbiol 7:1364

    Article  PubMed  PubMed Central  Google Scholar 

  97. Jo E, Seo G, Kwon JT, Lee M, Cheun Lee BC, Eom I, Kim P, Choi K (2013) Exposure to zinc oxide nanoparticles affects reproductive development and biodistribution in offspring rats. J Toxicol Sci 38:525–530

    Article  CAS  PubMed  Google Scholar 

  98. Kandeel M, Rehman TU, Akhtar T, Zaheer T, Ahmad S, Ashraf U, Omar M (2022) Antiparasitic applications of nanoparticles: a review. Pak Vet J 42(2):135–140. https://doi.org/10.29261/pakvetj/2022.040

  99. Khah MM, Ahmadi F, Amanlou H (2015) Influence of dietary different levels of zinc oxide nano particles on the yield and quality carcass of broiler chickens during starter stage. Indian J Anim Sci 85:287–290

    Article  Google Scholar 

  100. Khajeh BM, Afsharmanesh M, Salarmoini M, Tavakoli H (2018) Effect of zinc oxide nanoparticles and Bacillus coagulans as probiotic on growth, histomorphology of intestine, and immune parameters in broiler chickens. Comp Clin Path 27:399–406

    Article  Google Scholar 

  101. Khan I, Zaneb H, Masood S, Ashraf S, Rehman HF, Rehman HU, Ahmad S, Taj R, Salahuddin, Rahman SU (2022) Supplemental selenium nanoparticles-loaded to chitosan improves meat quality, pectoral muscle histology, tibia bone morphometry and tissue mineral retention in broilers. Pak Vet J 42(2):236–240. https://doi.org/10.29261/pakvetj/2022.007

  102. Khan RU, Naz S, Javdani M, Nikousefat Z, Selvaggi M, Tufarelli V, Laudadio V (2012) The use of turmeric (Curcuma longa) in poultry feed. Worlds Poult Sci J 68:97–103

    Article  Google Scholar 

  103. Khatami M, Alijani HQ, Heli H, Sharifi I (2018) Rectangular shaped zinc oxide nanoparticles: green synthesis by Stevia and its biomedical efficiency. Ceram Int 44:15596–15602

    Article  CAS  Google Scholar 

  104. Khater HF, Ziam H, Abbas A, Abbas RZ, Raza MA, Hussain K, Younis EZ, Radwan IT, Selim A (2020) Avian coccidiosis: recent advances in alternative control strategies and vaccine development. Agrobiol Rec 1:11–25

    Article  Google Scholar 

  105. Khoobbakht Z, Mohammadi M, Mehr MRA, Mohammadghasemi F, Sohani MM (2018) Comparative effects of zinc oxide, zinc oxide nanoparticle and zinc-methionine on hatchability and reproductive variables in male Japanese quail. Anim Reprod Sci 192:84–90

    Article  CAS  PubMed  Google Scholar 

  106. Khorsandi L, Heidari-Moghadam A, Jozi Z (2018) Nephrotoxic effects of low-dose zinc oxide nanoparticles in rats. J Nephropathol 7(3):158–165

    Article  Google Scholar 

  107. Kong T, Zhang SH, Zhang C, Zhang JL, Yang F, Wang GY, Yang ZJ, Bai DY, Shi YY, Liu TQ, Li HL (2020) The effects of 50 nm unmodified nano-ZnO on lipid metabolism and semen quality in male mice. Biol Trace Elem Res 194:432–442

    Article  CAS  PubMed  Google Scholar 

  108. Kosicki R, Błajet-Kosicka A, Grajewski J, Twarużek M (2016) Multiannual mycotoxin survey in feed materials and feedingstuffs. Anim Feed Sci Technol 215:165–180

    Article  CAS  Google Scholar 

  109. Król A, Pomastowski P, Rafińska K, Railean-Plugaru V, Buszewski B (2017) Zinc oxide nanoparticles: synthesis, antiseptic activity and toxicity mechanism. Adv Colloid Interface Sci 249:37–52

    Article  PubMed  Google Scholar 

  110. Kumar R, Roy I, Ohulchanskky TY, Vathy LA, Bergey EJ, Sajjad M, Prasad PN (2010) In vivo biodistribution and clearance studies using multimodal organically modified silica nanoparticles. ACS Nano 4:699–708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Kwiecień M, Winiarska-Mieczan A, Milczarek A, Klebaniuk R (2017) Biological response of broiler chickens to decreasing dietary inclusion levels of zinc glycine chelate. Biol Trace Elem Res 175:204–213

    Article  PubMed  Google Scholar 

  112. Lee SH, Wang TY, Hong JH, Cheng TJ, Lin CY (2016) NMR-based metabolomics to determine acute inhalation effects of nano-and fine-sized ZnO particles in the rat lung. Nanotoxicology 10:924–934

    Article  CAS  PubMed  Google Scholar 

  113. Li MZ, Huang JT, Tsai YH, Mao SY, Fu CM, Lien TF (2016) Nanosize of zinc oxide and the effects on zinc digestibility, growth performances, immune response and serum parameters of weanling piglets. Anim Sci J 87:1379–1385

    Article  CAS  PubMed  Google Scholar 

  114. Li LL, Gong YJ, Zhan HQ, Zheng YX, Zou XT (2019) Effects of dietary Zn-methionine supplementation on the laying performance, egg quality, antioxidant capacity, and serum parameters of laying hens. Poult Sci 98:923–931

    Article  CAS  PubMed  Google Scholar 

  115. Lin D, Xing B (2008) Root uptake and phytotoxicity of ZnO nanoparticles. Environ Sci Technol 42(15):5580–5585

    Article  CAS  PubMed  Google Scholar 

  116. Lin W, Xu Y, Huang CC, Ma Y, Shannon KB, Chen DR, Huang YW (2009) Toxicity of nano-and micro-sized ZnO particles in human lung epithelial cells. J Nanopart Res 11:25–39

    Article  CAS  Google Scholar 

  117. Lina T, Jianyang J, Fenghua Z, Huiying R, Wenli L (2009) Effect of nano-zinc oxide on the production and dressing performance of broiler. Chin Agric Sci Bull 02(003):318

    Google Scholar 

  118. Liou GY, Storz P (2010) Reactive oxygen species in cancer. Free Radic Res 44(5):479–496

    Article  CAS  PubMed  Google Scholar 

  119. Liu ZH, Lu L, Li SF, Zhang LY, Xi L, Zhang KY, Luo XG (2011) Effects of supplemental zinc source and level on growth performance, carcass traits, and meat quality of broilers. Poult Sci 90(8):1782–1790

    Article  CAS  PubMed  Google Scholar 

  120. Liu ZH, Lu L, Li SF, Zhang LY, Xi L, Zhang KY, Luo XG (2011) Effects of supplemental zinc source and level on growth performance, carcass traits, and meat quality of broilers. Poult Sci 90:1782–1790

    Article  CAS  PubMed  Google Scholar 

  121. Liu XQ, Zhang HF, Zhang WD, Zhang PF, Hao YN, Song R, Li L, Feng YN, Hao ZH, Shen W, Min LJ, Yang HD, Zhao Y (2016) Regulation of neuroendocrine cells and neuron factors in the ovary by zinc oxide nanoparticles. Toxicol Lett 256:19–32

    Article  CAS  PubMed  Google Scholar 

  122. Liu J, Kang Y, Yin S, Song B, Wei L, Chen L, Shao L (2017) Zinc oxide nanoparticles induce toxic responses in human neuroblastoma SHSY5Y cells in a size-dependent manner. Int J Nanomedicine 12:8085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Liu J, Zhao Y, Ge W, Zhang P, Liu X, Zhang W, Hao Y, Yu S, Li L, Chu M, Min L, Zhang H, Shen W (2017) Oocyte exposure to ZnO nanoparticles inhibits early embryonic development through the γ-H2AX and NF-κB signaling pathways. Oncotarget 8:42673

    Article  PubMed  PubMed Central  Google Scholar 

  124. Liu Z, Ren Z, Zhang J, Chuang CC, Kandaswamy E, Zhou T, Zuo L (2018) Role of ROS and nutritional antioxidants in human diseases. Front Physiol 9:477

    Article  PubMed  PubMed Central  Google Scholar 

  125. Liu H, Yang H, Fang Y, Li K, Tian L, Liu X, Zhang W, Tan Y, Lai W, Bian L, Lin B, Xi Z (2020) Neurotoxicity and biomarkers of zinc oxide nanoparticles in main functional brain regions and dopaminergic neurons. Sci Total Environ 705:135809

    Article  CAS  PubMed  Google Scholar 

  126. Lopes S, Ribeiro F, Wojnarowicz J, Łojkowski W, Jurkschat K, Crossley A, Soares AM, Loureiro S (2014) Zinc oxide nanoparticles toxicity to Daphnia magna: size-dependent effects and dissolution. Environ Toxicol Chem 33:190–198

    Article  CAS  PubMed  Google Scholar 

  127. Luo M, Shen C, Feltis BN, Martin LL, Hughes AE, Wright PF, Turney TW (2014) Reducing ZnO nanoparticle cytotoxicity by surface modification. Nanoscale 6:5791–5798

    Article  CAS  PubMed  Google Scholar 

  128. Ma DD, Yang WX (2016) Engineered nanoparticles induce cell apoptosis: potential for cancer therapy. Oncotarget 7:40882

    Article  PubMed  PubMed Central  Google Scholar 

  129. Ma H, Williams PL, Diamond SA (2013) Ecotoxicity of manufactured ZnO nanoparticles—a review. Environ Pollut 172:76–85

    Article  CAS  PubMed  Google Scholar 

  130. Ma B, Villalta PW, Balbo S, Stepanov I (2014) Analysis of a malondialdehyde–deoxyguanosine adduct in human leukocyte DNA by liquid chromatography nanoelectrospray–high-resolution tandem mass spectrometry. Chem Res Toxicol 27:1829–1836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Mabe I, Rapp C, Bain MM, Nys Y (2003) Supplementation of a corn-soybean meal diet with manganese, copper, and zinc from organic or inorganic sources improves eggshell quality in aged laying hens. Poult Sci 82:1903–1913

    Article  CAS  PubMed  Google Scholar 

  132. Mahmood F, Nawaz H, Khan SH, Yousaf M, Iqbal J (2022) Impact of supplemental exogenous lysolecithin on performance, fat digestibility, and lipid metabolites responses in broilers. Adv Life Sci 9(1):41–48

    Google Scholar 

  133. Mahmoud UT, Abdel-Mohsein HS, Mahmoud MA, Amen OA, Hassan RI, Abd-El-Malek AM, ... Osman MA (2020) Effect of zinc oxide nanoparticles on broilers’ performance and health status. Trop Anim Health Prod 52:2043–2054

  134. Malik F, Nawaz M, Anjum AA, Firyal S, Shahid MA, Irfan S, Ahmed F, Bhatti AA (2022) Molecular characterization of antibiotic resistance in poultry gut origin Enterococci and horizontal gene transfer of antibiotic resistance to Staphylococcus aureus. Pak Vet J 42(3):383–389. https://doi.org/10.29261/pakvetj/2022.035

  135. Mansouri E, Khorsandi L, Orazizadeh M, Jozi Z (2015) Dose-dependent hepatotoxicity effects of zinc oxide nanoparticles. Nanomed J 2:273–282

    CAS  Google Scholar 

  136. Martinez CR, Joshi P, Vera JL, Ramirez-Vick JE, Perales O, Singh SP (2011) Cytotoxic studies of PEG functionalized ZnO nanoparticles on MCF-7 cancer cells. In: NSTI Nanotechnol. Conf. Expo., NSTI-nanotech

  137. Mgbeahuruike AC, Ejioffor TE, Christian OC, Shoyinka VC, Karlsson M, Nordkvist E (2018) Detoxification of aflatoxin-contaminated poultry feeds by 3 adsorbents, bentonite, activated charcoal, and fuller’s earth. J Appl Poult Res 27:461–471

    Article  CAS  Google Scholar 

  138. Milani NC, Sbardella M, Ikeda NY, Arno A, Mascarenhas BC, Miyada VS (2017) Dietary zinc oxide nanoparticles as growth promoter for weanling pigs. Anim Feed Sci Technol 227:13–23

    Article  CAS  Google Scholar 

  139. Mir AH, Qamar A, Qadir I, Naqvi AH, Begum R (2020) Accumulation and trafficking of zinc oxide nanoparticles in an invertebrate model, Bombyx mori, with insights on their effects on immuno-competent cells. Sci Rep 10:1–14

    Article  Google Scholar 

  140. Mohammadi V, Ghazanfari S, Mohammadi-Sangcheshmeh A, Nazaran MH (2015) Comparative effects of zinc-nano complexes, zinc-sulphate and zinc-methionine on performance in broiler chickens. Br Poult Sci 56:486–493

    Article  CAS  PubMed  Google Scholar 

  141. Mohammed ET, Safwat GM (2013) Assessment of the ameliorative role of selenium nanoparticles on the oxidative stress of acetaminophen in some tissues of male albino rats. Beni Suef Univ J Basic Appl Sci 2:80–85

    Google Scholar 

  142. Mohd Yusof H, Mohamad R, Zaidan UH, Rahman A (2019) Microbial synthesis of zinc oxide nanoparticles and their potential application as an antimicrobial agent and a feed supplement in animal industry: a review. J Anim Sci Biotechnol 10:1–22

    Article  CAS  Google Scholar 

  143. Mohsin M, Li L, Huang X et al (2021) Immunogenicity and protective efficacy of probiotics with EtIMP1C against Eimeria tenella challenge. Pak Vet J 41:274–278. https://doi.org/10.29261/pakvetj/2021.009

  144. Najafi M, Motevaseli E, Shirazi A, Geraily G, Rezaeyan A, Norouzi F, Rezapoor S, Abdollahi H (2018) Mechanisms of inflammatory responses to radiation and normal tissues toxicity: clinical implications. Int J Radiat Biol 94:335–356

    Article  CAS  PubMed  Google Scholar 

  145. Najafzadeh H, Ghoreishi SM, Mohammadian B, Rahimi E, Afzalzadeh MR, Kazemivarnamkhasti M, Ganjealidarani H (2013) Serum biochemical and histopathological changes in liver and kidney in lambs after zinc oxide nanoparticles administration. Vet World 6(8):534

    Article  Google Scholar 

  146. Nandi A, Yan LJ, Jana CK, Das N (2019) Role of catalase in oxidative stress-and age-associated degenerative diseases. Oxid Med Cell Longev 2019:1–19

    Article  Google Scholar 

  147. Naz S, Idris M, Khalique MA, Zia-Ur-Rahman, Alhidary IA, Abdelrahman MM, Khan RU, Chand N, Farooq U, Ahmad S (2016) The activity and use of zinc in poultry diets. World’s Poult Sci J 72(1):159–167

  148. Nys Y, Gautron J, Garcia-Ruiz JM, Hincke MT (2004) Avian eggshell mineralization: biochemical and functional characterization of matrix proteins. C R Palevol 3:549–562

    Article  Google Scholar 

  149. Onnainty R, Onida B, Páez P, Longhi M, Barresi A, Granero G (2016) Targeted chitosan-based bionanocomposites for controlled oral mucosal delivery of chlorhexidine. Int J Pharm 509:408–418

    Article  CAS  PubMed  Google Scholar 

  150. Onunkwo DN, Jabbar A, Talha M, Rauf A, Javaid H, Munir MU, Irm N, Saleem MH (2021) Response of starter broiler chickens to feed diets treated with organic acids. Adv Life Sci 8(3):257–261

    CAS  Google Scholar 

  151. Ostrovsky S, Kazimirsky G, Gedanken A, Brodie C (2009) Selective cytotoxic effect of ZnO nanoparticles on glioma cells. Nano Res 2:882–890

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  153. Pati R, Das I, Mehta RK, Sahu R, Sonawane A (2016) Zinc-oxide nanoparticles exhibit genotoxic, clastogenic, cytotoxic and actin depolymerization effects by inducing oxidative stress responses in macrophages and adult mice. Toxicol Sci 150:454–472

    Article  CAS  PubMed  Google Scholar 

  154. Patra A, Lalhriatpuii M (2020) progress and prospect of essential mineral nanoparticles in poultry nutrition and feeding—a review. Biol Trace Elem Res 197:233–253

    Article  CAS  PubMed  Google Scholar 

  155. Perera NCN, Godahewa GI, Lee J (2016) Copper-zinc-superoxide dismutase (CuZnSOD), an antioxidant gene from seahorse (Hippocampus abdominalis); molecular cloning, sequence characterization, antioxidant activity and potential peroxidation function of its recombinant protein. Fish Shellfish Immunol 57:386–399

    Article  CAS  PubMed  Google Scholar 

  156. Piccinno F, Gottschalk F, Seeger S, Nowack B (2012) Industrial production quantities and uses of ten engineered nanomaterials in Europe and the world. J Nanopart Res 14:1–11

    Article  Google Scholar 

  157. Pinho AR, Rebelo S, Pereira MDL (2020) The impact of zinc oxide nanoparticles on male (in) fertility. Materials 13:849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Poynton HC, Lazorchak JM, Impellitteri CA, Smith ME, Rogers K, Patra M, ... Vulpe CD (2011) Differential gene expression in Daphnia magna suggests distinct modes of action and bioavailability for ZnO nanoparticles and Zn ions. Environ Sci Technol 45:762–768

  159. Prasad AS (2014) Zinc: an antioxidant and anti-inflammatory agent: role of zinc in degenerative disorders of aging. J Trace Elem Med Biol 28:364–371

    Article  CAS  PubMed  Google Scholar 

  160. Premanathan M, Karthikeyan K, Jeyasubramanian K, Manivannan G (2011) Selective toxicity of ZnO nanoparticles toward Gram-positive bacteria and cancer cells by apoptosis through lipid peroxidation. Nanomed: Nanotechnol Biol Med 7(2):184–192

  161. Pujalté I, Passagne I, Brouillaud B, Tréguer M, Durand E, Ohayon-Courtès C, l’Azou B (2011) Cytotoxicity and oxidative stress induced by different metallic nanoparticles on human kidney cells. Part Fibre Toxicol 8:1–16

    Article  Google Scholar 

  162. Pulit-Prociak J, Chwastowski J, Kucharski A, Banach M (2016) Functionalization of textiles with silver and zinc oxide nanoparticles. Appl Surf Sci 385:543–553

    Article  CAS  Google Scholar 

  163. Qiao Y, Liang X, Yan Y, Lu Y, Zhang D, Yao W, Wu W, Yan Z (2018) Identification of exosomal miRNAs in rats with pulmonary neutrophilic inflammation induced by zinc oxide nanoparticles. Front Physiol 9:217

    Article  PubMed  PubMed Central  Google Scholar 

  164. Qing X, Shi D, Lv X, Wang B, Chen S, Shao Z (2019) Prognostic significance of 8-hydroxy-2′-deoxyguanosine in solid tumors: a meta-analysis. BMC Cancer 19:1–15

    Article  CAS  Google Scholar 

  165. Wajiha, Qureshi NA, Afridi R (2018) Comparative analysis of egg adapted vaccines and salinomycin against coccidiosis in chicks. Microb Pathog 123:454–460

  166. Rajendran D (2013) Application of nano minerals in animal production system. Res J Biotechnol 8:1–3

    CAS  Google Scholar 

  167. Rajput VD, Minkina TM, Behal A, Sushkova SN, Mandzhieva S, Singh R, ... Movsesyan HS (2018) Effects of zinc-oxide nanoparticles on soil, plants, animals and soil organisms: A review. Environ Nanotechnol Monitor Manag 9:76–84

  168. Ramasamy M, Das M, An SSA, Yi DK (2014) Role of surface modification in zinc oxide nanoparticles and its toxicity assessment toward human dermal fibroblast cells. Int J Nanomedicine 9:3707

    CAS  PubMed  PubMed Central  Google Scholar 

  169. Rasmussen JW, Martinez E, Louka P, Wingett DG (2010) Zinc oxide nanoparticles for selective destruction of tumor cells and potential for drug delivery applications. Expert Opin Drug Deliv 7(9):1063–1077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Raza W, Faisal SM, Owais M, Bahnemann D, Muneer M (2016) Facile fabrication of highly efficient modified ZnO photocatalyst with enhanced photocatalytic, antibacterial and anticancer activity. RSC Adv 6(82):78335–78350

    Article  CAS  Google Scholar 

  171. Raza QS, Saleemi MK, Gul ST, Irshad H, Fayyaz A, Zaheer I, Tahir MW, Fatima Z, Chohan TZ, Imran M, Ali H, Khalid HMS, Jamil M, Zaheer MI, Khan A (2022) Role of essential oils/volatile oils in poultry production—a review on present, past and future contemplations. Agrobiol Rec 7:40–56

    Google Scholar 

  172. Reda FM, El-Saadony MT, El-Rayes TK, Attia AI, El-Sayed SA, Ahmed SY, ... Alagawany M (2021) Use of biological nano zinc as a feed additive in quail nutrition: biosynthesis, antimicrobial activity and its effect on growth, feed utilisation, blood metabolites and intestinal microbiota. Ital J Anim Sci 20:324–335

  173. Rodríguez-Navarro AB, Marie P, Nys Y, Hincke MT, Gautron J (2015) Amorphous calcium carbonate controls avian eggshell mineralization: a new paradigm for understanding rapid eggshell calcification. J Struct Biol 190:291–303

    Article  PubMed  Google Scholar 

  174. Rosi NL, Mirkin CA (2005) Nanostructures in biodiagnostics. Chem Rev 105:1547–1562

    Article  CAS  PubMed  Google Scholar 

  175. Sadoval M, Henry P, Littell R, Miles R, Butcher G, Am-merman C (1999) Effect of dietary zinc source and method of oral administration on performance and tissue trace mineral concentration of broiler chicks. J Anim Sci 77:1788–1799

    Article  CAS  PubMed  Google Scholar 

  176. Sagar PD, Mandal AB, Akbar N, Dinani OP (2018) Effect of different levels and sources of zinc on growth performance and immunity of broiler chicken during summer. Int J Curr Microbiol Appl Sc 7(05):459–471

    Article  Google Scholar 

  177. Sahoo A, Swain RK, Mishra SK (2014) Effect of inorganic, organic and nano zinc supplemented diets on bioavailability and immunity status of broilers. Int J Adv Res 2(11):828–837

    Google Scholar 

  178. Saleh AA (2014) Effect of dietary mixture of Aspergillus probiotic and selenium nano-particles on growth, nutrient digestibilities, selected blood parameters and muscle fatty acid profile in broiler chickens. Anim Sci Pap Rep 32:65–79

    CAS  Google Scholar 

  179. Saliani M, Jalal R, Goharshadi EK (2016) Mechanism of oxidative stress involved in the toxicity of ZnO nanoparticles against eukaryotic cells. Nanomed J 3:1–14

    CAS  Google Scholar 

  180. Saman S, Moradhaseli S, Shokouhian A, Ghorbani M (2013) Histopathological effects of ZnO nanoparticles on liver and heart tissues in wistar rats. Adv Biores 4:83–88

    CAS  Google Scholar 

  181. Samiullah S, Omar AS, Roberts JR, Chousalkar K (2014) Effect of production system and flock age on egg quality. In: Proceedings of the 27th Annual Australian Poultry Science Symposium, Sydney, New South Wales, pp 133–136

  182. Samy A, Hassan HMA, Elsherif HMR (2022) Effect of nano zinc oxide and traditional zinc (oxide and sulphate) sources on performance, bone characteristics and physiological parameters of broiler chicks. Int J Vet Sci 11(4):486–492

    Google Scholar 

  183. Saptarshi SR, Feltis BN, Wright PF, Lopata AL (2015) Investigating the immunomodulatory nature of zinc oxide nanoparticles at sub-cytotoxic levels in vitro and after intranasal instillation in vivo. J Nanobiotechnology 13:1–11

    Article  Google Scholar 

  184. Saravanan M, Gopinath V, Chaurasia MK, Syed A, Ameen F, Purushothaman N (2018) Green synthesis of anisotropic zinc oxide nanoparticles with antibacterial and cytofriendly properties. Microb Pathog 115:57–63

    Article  CAS  PubMed  Google Scholar 

  185. Sarkar J, Ghosh M, Mukherjee A, Chattopadhyay D, Acharya K (2014) Biosynthesis and safety evaluation of ZnO nanoparticles. Bioprocess Biosyst Eng 37:165–171

    Article  CAS  PubMed  Google Scholar 

  186. Saxena R, Batra J (2020) Arthritis as a disease of aging and changes in antioxidant status. In: Aging. Academic Press, pp 83–94

  187. Schlegel P, Sauvant D, Jondreville C (2013) Bioavailability of zinc sources and their interaction with phytates in broilers and piglets. Animal 7:47–59

    Article  CAS  PubMed  Google Scholar 

  188. Seil JT, Webster TJ (2012) Antimicrobial applications of nanotechnology: methods and literature. Int J Nanomedicine 7:2767

    CAS  PubMed  PubMed Central  Google Scholar 

  189. Shahzad K, Khan MN, Jabeen F, Kosour N, Chaudhry AS, Sohail M, Ahmad N (2019) Toxicity of zinc oxide nanoparticles (ZnO-NPs) in tilapia (Oreochromis mossambicus): tissue accumulation, oxidative stress, histopathology and genotoxicity. IJEST 16:1973–1984

    CAS  Google Scholar 

  190. Shao Y, Lei Z, Yuan J, Yang Y, Guo Y, Zhang B (2014) Effect of zinc on growth performance, gut morphometry, and cecal microbial community in broilers challenged with Salmonella enterica serovar typhimurium. J Microbiol 52:1002–1011

    Article  CAS  PubMed  Google Scholar 

  191. Sharma V, Singh P, Pandey AK, Dhawan A (2012) Induction of oxidative stress, DNA damage and apoptosis in mouse liver after sub-acute oral exposure to zinc oxide nanoparticles. Mutat Res Genet Toxicol Environ Mutagen 745:84–91

    Article  CAS  Google Scholar 

  192. Shnawa BH, Jalil PJ, Aspoukeh PK, Mohammed DA, Biro DM (2022) Protoscolicidal and biocompatibility properties of biologically fabricated zinc oxide nanoparticles using Ziziphus spina-christi leaves. Pak Vet J 42(4):517–525. https://doi.org/10.29261/pakvetj/2022.058

  193. Shrivastava S, Bera T, Roy A, Singh G, Ramachandrarao P, Dash D (2007) Characterization of enhanced antibacterial effects of novel silver nanoparticles. Nanotechnology 18(22):225103

  194. Siddique T, Deng HX, Ajroud-Driss S (2013) Motor neuron disease. In: Emery and Rimoin's Principles and Practice of Medical Genetics. pp 1–22

  195. Sinha R, Karan R, Sinha A, Khare SK (2011) Interaction and nanotoxic effect of ZnO and Ag nanoparticles on mesophilic and halophilic bacterial cells. Bioresour Technol 102:1516–1520

    Article  CAS  PubMed  Google Scholar 

  196. Sirelkhatim A, Mahmud S, Seeni A, Kaus NHM, Ann LC, Bakhori SKM, Hasan H, Mohamad D (2015) Review on zinc oxide nanoparticles: antibacterial activity and toxicity mechanism. Nanomicro Lett 7:219–242

    CAS  PubMed  Google Scholar 

  197. Sisubalan N, Ramkumar VS, Pugazhendhi A, Karthikeyan C, Indira K, Gopinath K, ... Basha MHG (2018) ROS-mediated cytotoxic activity of ZnO and CeO 2 nanoparticles synthesized using the Rubia cordifolia L. leaf extract on MG-63 human osteosarcoma cell lines. Environ Sci Pollut Res 25:10482–10492

  198. Smaoui S, Chérif I, Hlima HB, Khan MU, Rebezov M, Thiruvengadam M, Sarkar T, Shariati MA, Lorenzo JM (2023) Zinc oxide nanoparticles in meat packaging: a systematic review of recent literature. Food Packag Shelf Life 36:101045

  199. Soren S, Kumar S, Mishra S, Jena PK, Verma SK, Parhi P (2018) Evaluation of antibacterial and antioxidant potential of the zinc oxide nanoparticles synthesized by aqueous and polyol method. Microb Pathog 119:145–151

    Article  CAS  PubMed  Google Scholar 

  200. Sri Sindhura K, Prasad TNVKV, Panner SP, Hussain OM (2014) Synthesis, characterization and evaluation of effect of phytogenic zinc nanoparticles on soil exo-enzymes. Appl Nanosci 4:819–827

    Article  CAS  Google Scholar 

  201. Sukhanova A, Bozrova S, Sokolov P, Berestovoy M, Karaulov A, Nabiev I (2018) Dependence of nanoparticle toxicity on their physical and chemical properties. Nanoscale Res Lett 13:1–21

    Article  CAS  Google Scholar 

  202. Suttle NF (2022) Mineral nutrition of livestock. Cabi

  203. Swain PS, Rao SB, Rajendran D, Dominic G, Selvaraju S (2016) Nano zinc, an alternative to conventional zinc as ani-mal feed supplement: A review. Anim Nutr 2:134–141

    Article  PubMed  PubMed Central  Google Scholar 

  204. Taccola L, Raffa V, Riggio C, Vittorio O, Iorio MC, Vanacore R, ... Cuschieri A (2011) Zinc oxide nanoparticles as selective killers of proliferating cells. Int J Nanomed 1129–1140

  205. Tahir A, Khan MA, Bibi K, Bibi S, Rauf F, Ayaz F (2021) Prevalence of colibacillosis in young broiler chicks and antibiogram of Escherichia coli in different areas of Hazara region. Adv Life Sci 8(3):238–240

    CAS  Google Scholar 

  206. Talebi AR, Khorsandi L, Moridian M (2013) The effect of zinc oxide nanoparticles on mouse spermatogenesis. J Assist Reprod Genet 30:1203–1209

    Article  PubMed  PubMed Central  Google Scholar 

  207. Tammam AM, Ibrahim SA, Hemid AA, Abdel-Azeem F, Salem W (2020) Effect of nanoparticles supplementation in broiler diets on performance, microbial population and digestive tract measurements. Int J Vet Sci 9:373–378

    Google Scholar 

  208. Tang HQ, Xu M, Rong Q, Jin RW, Liu QJ, Li YL (2016) The effect of ZnO nanoparticles on liver function in rats. Int J Nanomedicine 11:4275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  209. Thurber A, Wingett DG, Rasmussen JW, Layne J, Johnson L, Tenne DA, ... Punnoose A (2012) Improving the selective cancer killing ability of ZnO nanoparticles using Fe doping. Nanotoxicology 6(4):440–452

  210. Titma T, Shimmo R, Siigur J, Kahru A (2016) Toxicity of antimony, copper, cobalt, manganese, titanium and zinc oxide nanoparticles for the alveolar and intestinal epithelial barrier cells in vitro. Cytotechnology 68:2363–2377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  211. Travel A, Nys Y, Bain M (2011) Effect of hen age, moult, laying environment and egg storage on egg quality. In: Improving the safety and quality of eggs and egg products. Woodhead Publishing, pp 300–329

  212. Tsai YH, Mao SY, Li MZ, Huang JT, Lien TF (2016) Effects of nanosize zinc oxide on zinc retention, eggshell quality, immune response and serum parameters of aged laying hens. Anim Feed Sci Technol 213:99–107

    Article  CAS  Google Scholar 

  213. Umair M, Altaf S, Muzaffar H, Iftikhar A, Ali A, Batool N, Iqbal T, Saif-ur-Rehman BSR (2022) Green nanotechnology mediated silver and iron oxide nanoparticles: Potential antimicrobials. Agrobiol Rec 10:35–41

    Article  Google Scholar 

  214. Vila-Donat P, Marín S, Sanchis V, Ramos AJ (2018) A review of the mycotoxin adsorbing agents, with an emphasis on their multi-binding capacity, for animal feed decontamination. Food Chem Toxicol 114:246–259

    Article  CAS  PubMed  Google Scholar 

  215. Vinardell MP, Mitjans M (2015) Antitumor activities of metal oxide nanoparticles. Nanomaterials 5(2):1004–1021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  216. Wahab R, Kaushik N, Khan F, Kaushik NK, Choi EH, Musarrat J, Al-Khedhairy AA (2016) Self-styled ZnO nanostructures promotes the cancer cell damage and supresses the epithelial phenotype of glioblastoma. Sci Rep 6:1–13

    Article  Google Scholar 

  217. Wan Y, Zhang B (2022) The impact of zinc and zinc homeostasis on the intestinal mucosal barrier and intestinal diseases. Biomolecules 12:900

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  218. Wang C, Zhang L, Ying Z, He J, Zhou L, Zhang L, ... Wang T (2018) Effects of dietary zinc oxide nanoparticles on growth, diarrhea, mineral deposition, intestinal morphology, and barrier of weaned piglets. Biol Trace Elem Res 185:364–374

  219. Wang B, Feng WY, Wang TC, Jia G, Wang M, Shi JW, ... Chai ZF (2006) Acute toxicity of nano-and micro-scale zinc powder in healthy adult mice. Toxicol Lett 161:115–123

  220. Wang B, Feng W, Wang M, Wang T, Gu Y, Zhu M, ... Wang J (2008) Acute toxicological impact of nano-and submicro-scaled zinc oxide powder on healthy adult mice. J Nanopart Res 10:263–276

  221. Wang HJ, Growcock AC, Tang TH, O’Hara J, Huang YW, Aronstam RS (2010) Zinc oxide nanoparticle disruption of store-operated calcium entry in a muscarinic receptor signaling pathway. Toxicol in Vitro 24:1953–1961

    Article  CAS  PubMed  Google Scholar 

  222. Wang C, Lu J, Zhou L, Li J, Xu J, Li W, Wang T (2016) Effects of long-term exposure to zinc oxide nanoparticles on development, zinc metabolism and biodistribution of minerals (Zn, Fe, Cu, Mn) in mice. PLoS ONE 11:e0164434

    Article  PubMed  PubMed Central  Google Scholar 

  223. Wang C, Zhang L, Su W, Ying Z, He J, Zhang L, Wang T (2017a) Zinc oxide nanoparticles as a substitute for zinc oxide or colistin sulfate: effects on growth, serum enzymes, zinc deposition, intestinal morphology and epithelial barrier in weaned piglets. PLoS ONE 12:e0181136

    Article  PubMed  PubMed Central  Google Scholar 

  224. Wang D, Li H, Liu Z, Zhou J, Zhang T (2017b) Acute toxicological effects of zinc oxide nanoparticles in mice after intratracheal instillation. Int J Occup Environ Health 23:11–19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  225. Xia T, Kovochich M, Liong M, Madler L, Gilbert B, Shi H, ... Nel AE (2008) Comparison of the mechanism of toxicity of zinc oxide and cerium oxide nanoparticles based on dissolution and oxidative stress properties. ACS Nano 2:2121–2134

  226. Xia T, Lai W, Han M, Han M, Ma X, Zhang L (2017) Dietary ZnO nanoparticles alters intestinal microbiota and inflammation response in weaned piglets. Oncotarget 8:64878

    Article  PubMed  PubMed Central  Google Scholar 

  227. Xiaoli F, Junrong W, Xuan L, Yanli Z, Limin W, Jia L, Longquan S (2017) Prenatal exposure to nanosized zinc oxide in rats: neurotoxicity and postnatal impaired learning and memory ability. Nanomedicine 12:777–795

    Article  PubMed  Google Scholar 

  228. Xueting L, Rehman MU, Zhang H, Tian X, Wu X, Mehmood K, Zhou D (2018) Protective effects of nano-elemental selenium against chromium-vi-induced oxidative stress in broiler liver. J Biol Regul Homeost Agents 32:47–54

    CAS  PubMed  Google Scholar 

  229. Yan G, Huang Y, Bu Q, Lv L, Deng P, Zhou J, ... Zhao Y (2012) Zinc oxide nanoparticles cause nephrotoxicity and kidney metabolism alterations in rats. J Environ Sci Health A Environ Sci Eng Toxic Hazard Subst Control 47:577–588

  230. Yang J, Bai F, Zhang K, Bai S, Peng X, Ding X, ... Zhao L (2012) Effects of feeding corn naturally contaminated with aflatoxin B1 and B2 on hepatic functions of broilers. Poult Sci 91:2792–2801

  231. Yang Y, Zhang C, Hu Z (2013) Impact of metallic and metal oxide nanoparticles on wastewater treatment and anaerobic digestion. Environ Sci Process Impacts 15(1):39–48

    Article  CAS  PubMed  Google Scholar 

  232. Yausheva E, Miroshnikov S, Sizova E (2018) Intestinal microbiome of broiler chickens after use of nanoparticles and metal salts. Environ Sci Pollut Res Int 25:18109–18120

    Article  CAS  PubMed  Google Scholar 

  233. Yousef MI, Al-Hamadani M, Kamel MA (2019) Reproductive toxicity of aluminum oxide nanoparticles and zinc oxide nanoparticles in male rats. Nanoparticle 1:3

    Google Scholar 

  234. Youssef FS, Elbanna HA, Elzorba HY, Galal AM, Mohamed G, Ismail SH (2020) Synthesis and characterization of florfenicol-silver nanocomposite and its antibacterial activity against some gram positive and gram-negative bacteria. Int J Vet Sci 9:324–330

    Google Scholar 

  235. Yung M, Fougères PA, Leung YH, Liu F, Djurišić AB, Giesy JP, Leung KM (2017) Physicochemical characteristics and toxicity of surface-modified zinc oxide nanoparticles to freshwater and marine microalgae. Sci Rep 7:1–14

    Article  Google Scholar 

  236. Zaheer T, Kandeel M, Abbas RZ, Khan SR, Rehman Tu, Aqib AI (2022) Acaricidal potential and ecotoxicity of metallic nano-pesticides used against the major life stages of Hyalomma ticks. Life 12:977. https://doi.org/10.3390/life12070977

  237. Zhai QY, Ge W, Wang JJ, Sun XF, Ma JM, Liu JC, ... Shen W (2018) Exposure to Zinc oxide nanoparticles during pregnancy induces oocyte DNA damage and affects ovarian reserve of mouse offspring. Aging (Albany NY) 10:2170

  238. Zhang L, Jiang Y, Ding Y, Daskalakis N, Jeuken L, Povey M, ... York DW (2010) Mechanistic investigation into antibacterial behaviour of suspensions of ZnO nanoparticles against E. coli. J Nanopart Res 12:1625–1636

  239. Zhang W, Zhao Y, Li F, Li L, Feng Y, Min L, Ma D, Yu S, Liu J, Zhang H, Shi T, Li F, Shen W (2018) Zinc oxide nanoparticle caused plasma metabolomic perturbations correlate with hepatic steatosis. Front Pharmacol 9:57

    Article  PubMed  PubMed Central  Google Scholar 

  240. Zhao Y, Li L, Zhang PF, Shen W, Liu J, Yang FF, ... Hao ZH (2015) Differential regulation of gene and protein expression by zinc oxide nanoparticles in hen’s ovarian granulosa cells: specific roles of nanoparticles. PLoS One 10:e0140499

  241. Zhao Y, Li L, Zhang PF, Liu XQ, Zhang WD, Ding ZP, ... Hao ZH (2016) Regulation of egg quality and lipids metabolism by Zinc Oxide Nanoparticles. Poult Sci 95:920–933

  242. Zhao X, Wang S, Wu Y, You H, Lv L (2013) Acute ZnO nanoparticles exposure induces developmental toxicity, oxidative stress and DNA damage in embryo-larval zebrafish. Aquat Toxicol 136:49–59

    Article  PubMed  Google Scholar 

  243. 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

    Article  CAS  PubMed  Google Scholar 

  244. Zhou J, Xu NS, Wang ZL (2006) Dissolving behavior and stability of ZnO wires in biofluids: a study on biodegradability and biocompatibility of ZnO nanostructures. Adv Mater 18(18):2432–2435

    Article  CAS  Google Scholar 

Download references

Funding

There is no specific research funding involved in the execution of this work; therefore, central laboratory facilities insisted us for novel of research performance and report to this journal.

Author information

Authors and Affiliations

  1. Institute of Microbiology, University of Agriculture, Faisalabad, Pakistan

    Arjmand Fatima, Sultan Ali & Muhammad Shahid Mahmood

  2. Institute of Parasitology, University of Agriculture, Faisalabad, Pakistan

    Tean Zaheer & Rao Zahid Abbas

  3. University Center for Research and Development (UCRD), Department of Physics, Chandigarh University, Mohali, Gharuan, Punjab, 140413, India

    Kaushik Pal

  4. KBCMA College of Veterinary and Animal Sciences, Sub-Campus UVAS-Lahore, Narowal, Pakistan

    Tayyaba Akhtar

Authors
  1. Arjmand Fatima
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tean Zaheer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kaushik Pal
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rao Zahid Abbas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tayyaba Akhtar
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sultan Ali
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Muhammad Shahid Mahmood
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

This manuscript not submitted elsewhere for publication as well as the author’s contribution mentioned below;

Arjmand Fatima: manuscript writing and experimental data investigations and analysis. Tean Zaheer: experimental data analysis and have been involved in drafting the manuscript or revising it critically for important intellectual content. Kaushik Pal: plan of research direction and supervision for the execution of experimental analysis and draft moderation with submission. Rao Zahid Abbas: mentorship guidance and supervision, as well as resources of common research facilities of experimental investigations through central facilities. Tayyaba Akhtar: substantial contributions to conception and design, or acquisition of data, or analysis and interpretation of data. Sultan Ali: accountable for all aspects of the work in ensuring that experiment related to the accuracy or integrity of any part of the work is appropriately investigated and resolved. Muhammad Shahid Mahmood: throughout experimental data checking as well as exploration for the final round revision.

Corresponding authors

Correspondence to Kaushik Pal or Rao Zahid Abbas.

Ethics declarations

Competing Interests

The authors declare no competing interests.

Additional information

Publisher's Note

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

Highlights

• Cutting edge nanomaterials research in poultry has revolutionized over the last decades.

• ZnO itself and ZnO nanoparticles are known to regulate health and productivity in chickens.

• Toxicological aspect of ZnO NPs use in poultry needs future research direction.

• Materialization of toxicity studies due to ZnO can promote health and well-being of poultry and its consumers.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fatima, A., Zaheer, T., Pal, K. et al. Zinc Oxide Nanoparticles Significant Role in Poultry and Novel Toxicological Mechanisms. Biol Trace Elem Res 202, 268–290 (2024). https://doi.org/10.1007/s12011-023-03651-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-023-03651-x

Keywords

Search

Navigation