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Effects of Long-Term Dietary Zinc Oxide Nanoparticle on Liver Function, Deposition, and Absorption of Trace Minerals in Intrauterine Growth Retardation Pigs

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Abstract

To investigate the long-term effects of dietary zinc oxide nanoparticle (Nano-ZnO, 20–40 nm) on the relative organ weight, liver function, deposition, and absorption of trace minerals in intrauterine growth retardation (IUGR) pigs, piglets were allocated to NBW (6 normal birth weight piglets fed basal diets), IUGR (6 IUGR piglets fed basal diets) and IUGR+NZ (6 IUGR piglets fed basal diets + 600 mg Zn/kg from Nano-ZnO) groups at weaning (21 days of age), which were sampled at 163 days of age. There were no noteworthy changes in the relative weight of organs, hepatic histomorphology, serum alkaline phosphatase, glutamic pyruvic transaminase and glutamic oxalacetic transaminase activities, and Mn, Cu, and Fe concentrations in leg muscle, the liver, the tibia, and feces among the IUGR, NBW, and IUGR+NZ groups (P>0.05), and no intact Nano-ZnO in the jejunum, liver, and muscle was observed, while dietary Nano-ZnO increased the Zn concentrations in the tibia, the liver, serum, and feces (P<0.05) and mRNA expression of metallothionein (MT) 1A, MT2A, solute carrier family 39 member (ZIP) 4, ZIP14, ZIP8, divalent metal transporter 1, solute carrier family 30 member (ZnT) 1, ZnT4 and metal regulatory transcription factor 1, and ZIP8 protein expression in jejunal mucosa (P<0.05). Immunohistochemistry showed that dietary Nano-ZnO increased the relative optical density of ZIP8 (mainly expressed in cells of brush border) and MT2A (mainly expressed in villus lamina propria and gland/crypt) (P<0.05). In conclusion, long-term dietary Nano-ZnO showed no obvious side effects on the development of the major organs, liver function, and metabolism of Cu, Fe, and Mn in IUGR pigs, while it increased the Zn absorption and deposition via enhancing the expression of transporters (MT, ZIP, and ZnT families) in the jejunum, rather than via endocytosis as the form of intact nanoparticles.

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Data Availability

The data and materials of this study are available from the corresponding author upon reasonable request.

References

  1. Liao C, Jin Y, Li Y, Tjong SC (2020) Interactions of zinc oxide nanostructures with mammalian cells: cytotoxicity and photocatalytic toxicity. Int J Mol Sci 21:6305. https://doi.org/10.3390/ijms21176305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Singh T, Shukla S, Kumar P, Wahla V, Bajpai VK (2017) Application of nanotechnology in food science: perception and overview. Front Microbiol 8:1501. https://doi.org/10.3389/fmicb.2017.01501

    Article  PubMed  PubMed Central  Google Scholar 

  3. Singh TA, Sharma A, Tejwan N, Ghosh N, Das J, Sil PC (2021) A state of the art review on the synthesis, antibacterial, antioxidant, antidiabetic and tissue regeneration activities of zinc oxide nanoparticles. Adv Colloid Interface Sci 295:102495. https://doi.org/10.1016/j.cis.2021.102495

    Article  CAS  PubMed  Google Scholar 

  4. Singh TA, Das J, Sil PC (2020) Zinc oxide nanoparticles: a comprehensive review on its synthesis, anticancer and drug delivery applications as well as health risks. Adv Colloid Interface Sci 286:102317. https://doi.org/10.1016/j.cis.2020.102317

    Article  CAS  PubMed  Google Scholar 

  5. Mishra PK, Mishra H, Ekielski A, Talegaonkar S, Vaidya B (2017) Zinc oxide nanoparticles: a promising nanomaterial for biomedical applications. Drug Discov Today 22:1825–1834. https://doi.org/10.1016/j.drudis.2017.08.006

    Article  CAS  PubMed  Google Scholar 

  6. Ma H, Williams PL, Diamond SA (2013) Ecotoxicity of manufactured ZnO nanoparticles--a review. Environ Pollut 172:76–85. https://doi.org/10.1016/j.envpol.2012.08.011

    Article  CAS  PubMed  Google Scholar 

  7. Sun YB, Xia T, Wu H, Zhang WJ, Zhu YH, Xue JX, He DT, Zhang LY (2019) Effects of nano zinc oxide as an alternative to pharmacological dose of zinc oxide on growth performance, diarrhea, immune responses, and intestinal microflora profile in weaned piglets. Anim Feed Sci Technol 258:114312. https://doi.org/10.1016/j.anifeedsci.2019.114312

    Article  CAS  Google Scholar 

  8. Oh HJ, Park YJ, Cho JH, Song MH, Gu BH, Yun W, Lee JH, An JS, Kim YJ, Lee JS, Kim S, Kim H, Kim ES, Lee BK, Kim BW, Kim HB, Cho JH, Kim MH (2021) Changes in diarrhea score, nutrient digestibility, zinc utilization, intestinal immune profiles, and fecal microbiome in weaned piglets by different forms of zinc. Animals 11:1356. https://doi.org/10.3390/ani11051356

    Article  PubMed  PubMed Central  Google Scholar 

  9. Zhang J, Yu C, Li Z, Li J, Chen Y, Wang T, Wang C (2022) Effects of zinc oxide nanoparticles on growth, intestinal barrier, oxidative status and mineral deposition in 21-day-old broiler chicks. Biol Trace Elem Res 200:1826–1834. https://doi.org/10.1007/s12011-021-02771-6

    Article  CAS  PubMed  Google Scholar 

  10. 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 745:84–91. https://doi.org/10.1016/j.mrgentox.2011.12.009

    Article  CAS  PubMed  Google Scholar 

  11. Wang J, Zhu X, Guo Y, Wang Z, Zhao B, Yin Y, Liu G (2016) Influence of dietary copper on serum growth-related hormone levels and growth performance of weanling pigs. Biol Trace Elem Res 172:134–139. https://doi.org/10.1007/s12011-015-0574-2

    Article  CAS  PubMed  Google Scholar 

  12. Mahmoud MAM, Yahia D, Abdel-Magiud DS, Darwish MHA, Abd-Elkareem M, Mahmoud UT (2021) Broiler welfare is preserved by long-term low-dose oral exposure to zinc oxide nanoparticles: preliminary study. Nanotoxicology 15:605–620. https://doi.org/10.1080/17435390.2021.1905099

    Article  CAS  PubMed  Google Scholar 

  13. Wang C, Zhang L, Ying Z, He J, Zhou L, Zhang L, Zhong X, 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. https://doi.org/10.1007/s12011-018-1266-5

    Article  CAS  PubMed  Google Scholar 

  14. Wang C, Zhang L, Su W, Ying Z, He J, Zhang L, Zhong X, Wang T (2017) 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. https://doi.org/10.1371/journal.pone.0181136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Wu G, Bazer FW, Wallace JM, Spencer TE (2006) Board-invited review: intrauterine growth retardation: implications for the animal sciences. J Anim Sci 84:2316–2337. https://doi.org/10.2527/jas.2006-156

    Article  CAS  PubMed  Google Scholar 

  16. Zhang H, Chen Y, Li Y, Wang T (2020) Protective effect of polydatin on jejunal mucosal integrity, redox status, inflammatory response, and mitochondrial function in intrauterine growth-retarded weanling piglets. Oxid Med Cell Longev 2020:7178123. https://doi.org/10.1155/2020/7178123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Yun Y, Ji S, Yu G, Jia P, Niu Y, Zhang H, Zhang X, Wang T, Zhang L (2021) Effects of Bacillus subtilis on jejunal integrity, redox status, and microbial composition of intrauterine growth restriction suckling piglets. J Anim Sci 99:skab255. https://doi.org/10.1093/jas/skab255

    Article  PubMed  PubMed Central  Google Scholar 

  18. Yan E, Zhang J, Han H, Wu J, Gan Z, Wei C, Zhang L, Wang C, Wang T (2019) Curcumin alleviates IUGR jejunum damage by increasing antioxidant capacity through Nrf2/Keap1 pathway in growing pigs. Animals 10:41. https://doi.org/10.3390/ani10010041

    Article  PubMed  PubMed Central  Google Scholar 

  19. Zhou B, Zhang J, Liu H, Chen S, Wang T, Wang C (2022) Zinc oxide nanoparticle improves the intestinal function of intrauterine growth retardation finishing pigs via regulating intestinal morphology, inflammation, antioxidant status and autophagy. Front Vet Sci 9:884945. https://doi.org/10.3389/fvets.2022.884945

    Article  PubMed  PubMed Central  Google Scholar 

  20. Dong L, Zhong X, He J, Zhang L, Bai K, Xu W, Wang T, Huang X (2016) Supplementation of tributyrin improves the growth and intestinal digestive and barrier functions in intrauterine growth-restricted piglets. Clin Nutr 35:399–407. https://doi.org/10.1016/j.clnu.2015.03.002

    Article  CAS  PubMed  Google Scholar 

  21. Bacchetta R, Maran B, Marelli M, Santo N, Tremolada P (2016) Role of soluble zinc in ZnO nanoparticle cytotoxicity in Daphnia magna: a morphological approach. Environ Res 148:376–385. https://doi.org/10.1016/j.envres.2016.04.028

    Article  CAS  PubMed  Google Scholar 

  22. Santo N, Fascio U, Torres F, Guazzoni N, Tremolada P, Bettinetti R, Mantecca P, Bacchetta R (2014) Toxic effects and ultrastructural damages to Daphnia magna of two differently sized ZnO nanoparticles: does size matter? Water Res 53:339–350. https://doi.org/10.1016/j.watres.2014.01.036

    Article  CAS  PubMed  Google Scholar 

  23. Grecchi S, Malatesta M (2014) Visualizing endocytotic pathways at transmission electron microscopy via diaminobenzidine photo-oxidation by a fluorescent cell-membrane dye. Eur J Histochem 58:2449. https://doi.org/10.4081/ejh.2014.2449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Shrivastava R, Raza S, Yadav A, Kushwaha P, Flora SJ (2014) Effects of sub-acute exposure to TiO2, ZnO and Al2O3 nanoparticles on oxidative stress and histological changes in mouse liver and brain. Drug Chem Toxicol 37:336–347. https://doi.org/10.3109/01480545.2013.866134

    Article  CAS  PubMed  Google Scholar 

  25. Sahayam AC, Chaurasia SC, Venkateswarlu G (2010) Dry ashing of organic rich matrices with palladium for the determination of arsenic using inductively coupled plasma-mass spectrometry. Anal Chim Acta 661:17–19. https://doi.org/10.1016/j.aca.2009.12.010

    Article  CAS  PubMed  Google Scholar 

  26. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262

    Article  CAS  PubMed  Google Scholar 

  27. Cheng K, Yu C, Li Z, Li S, Yan E, Song Z, Zhang H, Zhang L, Wang T (2020) Resveratrol improves meat quality, muscular antioxidant capacity, lipid metabolism and fiber type composition of intrauterine growth retarded pigs. Meat Sci 170:108237. https://doi.org/10.1016/j.meatsci.2020.108237

    Article  CAS  PubMed  Google Scholar 

  28. Qi L, Jiang J, Zhang J, Zhang L, Wang T (2022) Effect of maternal curcumin supplementation on intestinal damage and the gut microbiota in male mice offspring with intra-uterine growth retardation. Eur J Nutr 61:1875–1892. https://doi.org/10.1007/s00394-021-02783-x

    Article  CAS  PubMed  Google Scholar 

  29. Wang QM, Huang XY, Guan WQ (2022) Expressions of interleukin-27 in oral lichen planus, oral leukoplakia, and oral squamous cell carcinoma. Inflammation 45:1023–1038. https://doi.org/10.1007/s10753-021-01599-5

    Article  CAS  PubMed  Google Scholar 

  30. Chen Y, Zhang Y, He J, Fu Y, Lin C, Li X (2017) MicroRNA-133b is regulated by TAp63 while no gene mutation is present in colorectal cancer. Oncol Rep 37:1646–1652. https://doi.org/10.3892/or.2017.5371

    Article  CAS  PubMed  Google Scholar 

  31. Michael B, Yano B, Sellers RS, Perry R, Morton D, Roome N, Johnson JK, Schafer K, Pitsch S (2007) Evaluation of organ weights for rodent and non-rodent toxicity studies: a review of regulatory guidelines and a survey of current practices. Toxicol Pathol 35:742–750. https://doi.org/10.1080/01926230701595292

    Article  PubMed  Google Scholar 

  32. Sellers RS, Morton D, Michael B, Roome N, Johnson JK, Yano BL, Perry R, Schafer K (2007) Society of Toxicologic Pathology position paper: organ weight recommendations for toxicology studies. Toxicol Pathol 35:751–755. https://doi.org/10.1080/01926230701595300

    Article  PubMed  Google Scholar 

  33. Wang C, Cheng K, Zhou L, He J, Zheng X, Zhang L, Zhong X, Wang T (2017) Evaluation of long-term toxicity of oral zinc oxide nanoparticles and zinc sulfate in mice. Biol Trace Elem Res 178:276–282. https://doi.org/10.1007/s12011-017-0934-1

    Article  CAS  PubMed  Google Scholar 

  34. Wang C, Lu J, Zhou L, Li J, Xu J, Li W, Zhang L, Zhong X, 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. https://doi.org/10.1371/journal.pone.0164434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Yasuno T, Okamoto H, Nagai M, Kimura S, Yamamoto T, Nagano K, Furubayashi T, Yoshikawa Y, Yasui H, Katsumi H, Sakane T, Yamamoto A (2011) The disposition and intestinal absorption of zinc in rats. Eur J Pharm Sci 44:410–415. https://doi.org/10.1016/j.ejps.2011.08.024

    Article  CAS  PubMed  Google Scholar 

  36. Cousins RJ (1986) Toward a molecular understanding of zinc metabolism. Clin Physiol Biochem 4(1):20–30

    CAS  PubMed  Google Scholar 

  37. Cheng K, Jia P, Ji S, Song Z, Zhang H, Zhang L, Wang T (2021) Improvement of the hepatic lipid status in intrauterine growth retarded pigs by resveratrol is related to the inhibition of mitochondrial dysfunction, oxidative stress and inflammation. Food Funct 12:278–290. https://doi.org/10.1039/d0fo01459a

    Article  CAS  PubMed  Google Scholar 

  38. Hill GM, Shannon MC (2019) Copper and zinc nutritional issues for agricultural animal production. Biol Trace Elem Res 188:148–159. https://doi.org/10.1007/s12011-018-1578-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Kociova S, Dolezelikova K, Horky P, Skalickova S, Baholet D, Bozdechova L, Vaclavkova E, Belkova J, Nevrkla P, Skladanka J, Do T, Zitka O, Haddad Y, Kopel P, Zurek L, Adam V, Smerkova K (2020) Zinc phosphate-based nanoparticles as alternatives to zinc oxide in diet of weaned piglets. J Anim Sci Biotechnol 11:59. https://doi.org/10.1186/s40104-020-00458-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Lukaski HC (2004) Vitamin and mineral status: effects on physical performance. Nutrition 20:632–644. https://doi.org/10.1016/j.nut.2004.04.001

    Article  CAS  PubMed  Google Scholar 

  41. Maggini S, Pierre A, Calder PC (2018) Immune function and micronutrient requirements change over the life course. Nutrients 10:1531. https://doi.org/10.3390/nu10101531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Hoffman HN 2nd, Phyliky RL, Fleming CR (1988) Zinc-induced copper deficiency. Gastroenterology 94:508–512. https://doi.org/10.1016/0016-5085(88)90445-3

    Article  PubMed  Google Scholar 

  43. Davin R, Manzanilla EG, Klasing KC, Pérez JF (2012) Evolution of zinc, iron, and copper concentrations along the gastrointestinal tract of piglets weaned with or without in-feed high doses of zinc oxide compared to unweaned littermates. J Anim Sci 4:248–250. https://doi.org/10.2527/jas.53999

    Article  Google Scholar 

  44. Rincker MJ, Hill GM, Link JE, Meyer AM, Rowntree JE (2005) Effects of dietary zinc and iron supplementation on mineral excretion, body composition, and mineral status of nursery pigs. J Anim Sci 83:2762–2774. https://doi.org/10.2527/2005.83122762x

    Article  CAS  PubMed  Google Scholar 

  45. Wang X, Zhou B (2010) Dietary zinc absorption: a play of zips and ZnTs in the gut. IUBMB Life 62:176–182. https://doi.org/10.1002/iub.291

    Article  CAS  PubMed  Google Scholar 

  46. Cousins RJ, Liuzzi JP, Lichten LA (2006) Mammalian zinc transport, trafficking, and signals. J Biol Chem 281:24085–24089. https://doi.org/10.1074/jbc.R600011200

    Article  CAS  PubMed  Google Scholar 

  47. Cousins RJ (1985) Absorption, transport, and hepatic metabolism of copper and zinc: special reference to metallothionein and ceruloplasmin. Physiol Rev 65:238–309. https://doi.org/10.1152/physrev.1985.65.2.238

    Article  CAS  PubMed  Google Scholar 

  48. Tran CD, Butler RN, Howarth GS, Philcox JC, Rofe AM, Coyle P (1999) Regional distribution and localization of zinc and metallothionein in the intestine of rats fed diets differing in zinc content. Scand J Gastroenterol 34:689–695. https://doi.org/10.1080/003655299750025895

    Article  CAS  PubMed  Google Scholar 

  49. Garrick MD, Dolan KG, Horbinski C, Ghio AJ, Higgins D, Porubcin M, Moore EG, Hainsworth LN, Umbreit JN, Conrad ME, Feng L, Lis A, Roth JA, Singleton S, Garrick LM (2003) DMT1: a mammalian transporter for multiple metals. Biometals 16:41–54. https://doi.org/10.1023/a:1020702213099

    Article  CAS  PubMed  Google Scholar 

  50. Garrick MD, Singleton ST, Vargas F, Kuo HC, Zhao L, Knöpfel M, Davidson T, Costa M, Paradkar P, Roth JA, Garrick LM (2006) DMT1: which metals does it transport? Biol Res 39:79–85. https://doi.org/10.4067/s0716-97602006000100009

    Article  CAS  PubMed  Google Scholar 

  51. Hardyman JE, Tyson J, Jackson KA, Aldridge C, Cockell SJ, Wakeling LA, Valentine RA, Ford D (2016) Zinc sensing by metal-responsive transcription factor 1 (MTF1) controls metallothionein and ZnT1 expression to buffer the sensitivity of the transcriptome response to zinc. Metallomics 8:337–343. https://doi.org/10.1039/c5mt00305a

    Article  CAS  PubMed  Google Scholar 

  52. Ling SC, Zhuo MQ, Zhang DG, Cui HY, Luo Z (2020) Nano-Zn increased Zn accumulation and triglyceride content by up-regulating lipogenesis in freshwater teleost, yellow catfish pelteobagrus fulvidraco. Int J Mol Sci 21:1615. https://doi.org/10.3390/ijms21051615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Chen SW, Lv WH, Wu K, Chen GH, Chen F, Song CC, Luo Z (2021) Dietary Nano-ZnO is absorbed via endocytosis and ZIP pathways, upregulates lipogenesis, and induces lipotoxicity in the intestine of yellow catfish. Int J Mol Sci 22:12047. https://doi.org/10.3390/ijms222112047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Melia JMP, Lin R, Xavier RJ, Thompson RB, Fu D, Wan F, Sears CL, Donowitz M (2019) Induction of the metal transporter ZIP8 by interferon gamma in intestinal epithelial cells: Potential role of metal dyshomeostasis in Crohn’s disease. Biochem Biophys Res Commun 515:325–331. https://doi.org/10.1016/j.bbrc.2019.05.137

    Article  CAS  PubMed  Google Scholar 

  55. Ensari A, Marsh MN (2018) Exploring the villus. Gastroenterol Hepatol Bed Bench 11(3):181–190. https://doi.org/10.22037/GHFBB.V0I0.1271

    Article  PubMed  PubMed Central  Google Scholar 

  56. Ishii M, Fukuoka Y, Deguchi S, Otake H, Tanino T, Nagai N (2019) Energy-dependent endocytosis is involved in the absorption of indomethacin nanoparticles in the small intestine. Int J Mol Sci 20:476. https://doi.org/10.3390/ijms20030476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Xu D, Ma Y, Han X, Chen Y (2021) Systematic toxicity evaluation of polystyrene nanoplastics on mice and molecular mechanism investigation about their internalization into Caco-2 cells. J Hazard Mater 417:126092. https://doi.org/10.1016/j.jhazmat.2021.126092

    Article  CAS  PubMed  Google Scholar 

  58. Beloqui A, des Rieux A, Preat V (2016) Mechanisms of transport of polymeric and lipidic nanoparticles across the intestinal barrier. Adv Drug Deliv Rev 106:242–255. https://doi.org/10.1016/j.addr.2016.04.014

    Article  CAS  PubMed  Google Scholar 

  59. Benmerah A, Lamaze C, Bègue B, Schmid SL, Dautry-Varsat A, Cerf-Bensussan N (1998) AP-2/Eps15 interaction is required for receptor-mediated endocytosis. J Cell Biol 140:1055–1062. https://doi.org/10.1083/jcb.140.5.1055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Khan I, Steeg PS (2021) Endocytosis: a pivotal pathway for regulating metastasis. Br J Cancer 124:66–75. https://doi.org/10.1038/s41416-020-01179-8

    Article  CAS  PubMed  Google Scholar 

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Funding

This study was supported by the National Natural Science Foundation of China (No.31972598).

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Authors and Affiliations

  1. College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, 210095, Jiangsu, China

    Binbin Zhou, Jian Li, Jiaqi Zhang, Huijuan Liu, Shun Chen, Tian Wang & Chao Wang

  2. Department of Animal Science, Jiangxi Biotech Vocational College, 608 Nanlian Road, Nanchang, 330200, Jiangxi, People’s Republic of China

    Yudan He

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  1. Binbin Zhou
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Contributions

Conceived and designed the experiment by Chao Wang and Tian Wang. Experiment preparation and data collection were performed by Binbin Zhou, Jian Li, Shun Chen, Huijuan Liu, Jiaqi Zhang, and Yudan He. Analyzed the data by Binbin Zhou. The first draft of the manuscript was writing by Binbin Zhou. Review and editing the first draft by Chao Wang. All authors have read and agreed to the published version of the manuscript.

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Zhou, B., Li, J., Zhang, J. et al. Effects of Long-Term Dietary Zinc Oxide Nanoparticle on Liver Function, Deposition, and Absorption of Trace Minerals in Intrauterine Growth Retardation Pigs. Biol Trace Elem Res 201, 4746–4757 (2023). https://doi.org/10.1007/s12011-022-03547-2

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