Skip to main content
Log in

Oxidative Stress and Neurotoxicity of Cadmium and Zinc on Artemia franciscana

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

Abstract

Despite not being redox-active metals, Cd and Zn can disrupt cellular redox homeostasis by acting pro-oxidatively. The aim of this study was to examine the effects of exposure to Zn (14 and 72 mg/L) and Cd (7.7 and 77 mg/L) for 24 and 48 h on oxidative and antioxidative parameters and the activity of glutathione-S-transferase in Artemia franciscana tissue. In addition, the neurotoxicity of the metals was examined by determining the activity of acetylcholinesterase (AChE). In A. franciscana tissue, Cd (0.0026 ± 0.0001 mg/L) was detected only after 48 h of exposure to 77 mg/L Cd. After 24 h, the 14- and 72-mg/L Zn treatments resulted in significant increases in the Zn concentration (0.54 ± 0.026 mg/L (p < 0.01) and 0.68 ± 0.035 (p < 0.0001), respectively) in A. franciscana tissue compared with the control level, and significant increases were also detected after 48 h (0.59 ± 0.02 (p < 0.0001) and 0.79 ± 0.015 (p < 0.0001), respectively). The malondialdehyde (MDA) concentration in the metal-treated samples was increased after 24 h of exposure, whereas after 48 h, an increase in the MDA concentration was detected only with 7.7. mg/L Cd. A significant increase in the H2O2 concentration after 24 h was measured only after treatment with 72 mg/L Zn. The treatment with 7.7 mg/L Cd for 24 h induced a significant increase in the AChE activity, whereas 48 h of treatment with 77 mg/L Cd and 14 mg/L Zn significantly inhibited AChE. The results indicate that lipid peroxidation resulting from metal toxicity may constitute the basis of neurotoxicity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data Availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable reques.

References

  1. Lane TW, Morel FM (2000) A biological function for cadmium in marine diatoms. Proc Natl Acad Sci USA 97(9):4627–4631. https://doi.org/10.1073/pnas.090091397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Rani A, Kumar A, Lal A, Pant M (2014) Cellular mechanisms of cadmium-induced toxicity: a review. Int J Environ Health Res 24(4):378–399. https://doi.org/10.1080/09603123.2013.835032

    Article  CAS  PubMed  Google Scholar 

  3. Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine. In: Halliwell B, Gutteridge JMC (eds) Free radicals in biology and medicine, 3rd edn. Oxford University Press, Oxford, pp 1–25

    Google Scholar 

  4. Marreiro DDN, Cruz KJC, Morais JBS, Beserra JB, Severo JS, De Oliveira ARS (2017) Zinc and oxidative stress: current mechanisms. Antioxidants 6(2):24. https://doi.org/10.3390/antiox6020024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Mousavi SR, Galavi M, Rezaei M (2013) Zinc (Zn) importance for crop production - a review. Int J Agron Plant Prod 4(1):64–68

    Google Scholar 

  6. Olechnowicz J, Tinkov A, Skalny A, Suliburska J (2018) Zinc status is associated with inflammation, oxidative stress, lipid, and glucose metabolism. J Physiol Sci 68(1):19–31. https://doi.org/10.1007/s12576-017-0571-7

    Article  CAS  PubMed  Google Scholar 

  7. Banaszak M, Górna I, Przysławski J (2021) Zinc and the innovative zinc-α2-glycoprotein adipokine play an ımportant role in lipid metabolism: a critical review. Nutrients 13(6):2023. https://doi.org/10.3390/nu13062023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Fosmire GJ (1990) Zinc toxicity. Am J Clin Nutr 51(2):225–227. https://doi.org/10.1093/ajcn/51.2.225

    Article  CAS  PubMed  Google Scholar 

  9. Hussain S, Khan M, Sheikh TMM, Mumtaz MZ, Chohan TA, Shamim S, Liu Y (2022) Zinc essentiality, toxicity, and ıts bacterial bioremediation: a comprehensive insight. Front Microbiol 13:900740. https://doi.org/10.3389/fmicb.2022.900740

    Article  PubMed  PubMed Central  Google Scholar 

  10. Li XF, Wang PF, Feng CL, Liu DQ, Chen JK, Wu FC (2019) Acute toxicity and hazardous concentrations of zinc to native freshwater organisms under different pH values in China. Bull Environ Contam Toxicol 103(1):120–126. https://doi.org/10.1007/s00128-018-2441-2

    Article  CAS  PubMed  Google Scholar 

  11. Zyadah MA, Abdel-Baky TE (2000) Toxicity and bioaccumulation of copper, zinc, and cadmium in some aquatic organisms. Bull Environ Contam Toxicol 64(5):740–747. https://doi.org/10.1007/s001280000066

    Article  CAS  PubMed  Google Scholar 

  12. Lee SR (2018) Critical role of zinc as either an antioxidant or a prooxidant in cellular systems. Oxid Med Cell Longev 2018:9156285. https://doi.org/10.1155/2018/9156285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Wang Y, Fang J, Leonard SS, Rao KMK (2004) Cadmium inhibits the electron transfer chain and induces reactive oxygen species. Free Radic Biol Med 36(11):1434–1443. https://doi.org/10.1016/j.freeradbiomed.2004.03.010

    Article  CAS  PubMed  Google Scholar 

  14. Wu H, Xuan R, Li Y, Zhang X, Wang Q, Wang L (2013) Effects of cadmium exposure on digestive enzymes, antioxidant enzymes, and lipid peroxidation in the freshwater crab Sinopotamon henanense. Environ Sci Pollut Res Int 20(6):4085–4092. https://doi.org/10.1007/s11356-012-1362-6

    Article  CAS  PubMed  Google Scholar 

  15. Trevisan R, Flesch S, Mattos JJ, Milani MR, Bainy ACD, Dafre AL (2014) Zinc causes acute impairment of glutathione metabolism followed by coordinated antioxidant defenses amplification in gills of brown mussels Perna perna. Comp Biochem Physiol C Toxicol Pharmacol 159:22–30. https://doi.org/10.1016/j.cbpc.2013.09.007

    Article  CAS  PubMed  Google Scholar 

  16. Sarasamma S, Audira G, Juniardi S, Sampurna BP, Liang S-T, Hao E, Lai Y-H, Hsiao C-D (2018) Zinc chloride exposure inhibits brain acetylcholine levels, produces neurotoxic signatures, and diminishes memory and motor activities in adult zebrafish. Int J Mol Sci 19(10):3195. https://doi.org/10.3390/ijms19103195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Zhang H, Reynolds M (2019) Cadmium exposure in living organisms: a short review. Sci Total Environ 678:761–767. https://doi.org/10.1016/j.scitotenv.2019.04.395

    Article  CAS  PubMed  Google Scholar 

  18. Thanan R, Oikawa S, Hiraku Y, Ohnishi S, Ma N, Pinlaor S, Yongvanit P, Kawanishi S, Murata M (2015) Oxidative stress and its significant roles in neurodegenerative diseases and cancer. Int J Mol Sci 16(1):193–217. https://doi.org/10.3390/ijms16010193

    Article  CAS  Google Scholar 

  19. Juan CA, Pérez de la Lastra JM, Plou FJ, Pérez-Lebeña E (2021) The chemistry of reactive oxygen species (ROS) revisited: outlining their role in biological macromolecules (dna, lipids and proteins) and ınduced pathologies. Int J Mol Sci 22(9):4642. https://doi.org/10.3390/ijms22094642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Deidda I, Russo R, Bonaventura R, Costa C, Zito F, Lampiasi N (2021) Neurotoxicity in marine invertebrates: an update. Biology 10(2):161. https://doi.org/10.3390/biology10020161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Gupta R, Shukla RK, Chandravanshi LP, Srivastava P, Dhuriya YK, Shanker J, Singh MP, Pant AB, Khanna VK (2017) Protective role of quercetin in cadmium-induced cholinergic dysfunctions in rat brain by modulating mitochondrial integrity and MAP kinase signaling. Mol Neurobiol 54(6):4560–4583. https://doi.org/10.1007/s12035-016-9950-y

    Article  CAS  PubMed  Google Scholar 

  22. Moyano P, de Frias M, Lobo M, Anadon MJ, Sola E, Pelayo A, Díaz MJ, Frejo MT, Del Pino J (2018) Cadmium induced ROS alters M1 and M3 receptors, leading to SN56 cholinergic neuronal loss, through AChE variants disruption. Toxicology 394:54–62. https://doi.org/10.1016/j.tox.2017.12.006

    Article  CAS  PubMed  Google Scholar 

  23. Grammou A, Papadimitriou C, Samaras P, Vasara E, Papadopoulos AI (2011) Effect of municipal waste water effluent upon the expression of glutathione S-transferase isoenzymes of brine shrimp Artemia. Chemosphere 84(1):105–109. https://doi.org/10.1016/j.chemosphere.2011.02.047

    Article  CAS  PubMed  Google Scholar 

  24. Ensibi C, Yahia MND (2017) Toxicity assessment of cadmium chloride on planktonic copepods Centropages ponticus using biochemical markers. Toxicol Rep 4:83–88. https://doi.org/10.1016/j.toxrep.2017.01.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Livingstone DR (2001) Contaminant-stimulated reactive oxygen production and oxidative damage in aquatic organisms. Mar Pollut Bull 42(8):656–666. https://doi.org/10.1016/S0025-326X(01)00060-1

    Article  CAS  PubMed  Google Scholar 

  26. Khaliq MA, James B, Chen YH, Saqib HSA, Li HH, Jayasuriya P, Guo W (2019) Uptake, translocation, and accumulation of Cd and its interaction with mineral nutrients (Fe, Zn, Ni, Ca, Mg) in upland rice. Chemosphere 215:916–924. https://doi.org/10.1016/j.chemosphere.2018.10.077

    Article  CAS  PubMed  Google Scholar 

  27. Zhang Y, Lu X, Wang N, Xin M, Geng S, Jia J, Meng Q (2016) Heavy metals in aquatic organisms of different trophic levels and their potential human health risk in Bohai Bay. China Environ Sci Pollut Res Int 23(17):17801–17810. https://doi.org/10.1007/s11356-016-6948-y

    Article  CAS  PubMed  Google Scholar 

  28. Rai PK, Lee SS, Zhang M, Tsang YF, Kim KH (2019) Heavy metals in food crops: health risks, fate, mechanisms, and management. Environ Int 125:365–385. https://doi.org/10.1016/j.envint.2019.01.067

    Article  CAS  PubMed  Google Scholar 

  29. Le Saux A, David E, Betoulle S, Bultelle F, Rocher B, Barjhoux I, Cosio C (2020) New insights in to cellular ımpacts of metals in aquatic animals. Environments 7(6):46. https://doi.org/10.3390/environments7060046

    Article  Google Scholar 

  30. Cavion F, Fusco L, Sosa S, Manfrin C, Alonso B, Zurutuza A, Della Loggia R, Tubaro A, Prato M, Pelin M (2020) Ecotoxicological impact of graphene oxide: toxic effects on the model organism Artemia franciscana. Environ Sci Nano 7:3605–3615. https://doi.org/10.1039/d0en00747a

    Article  CAS  Google Scholar 

  31. Nunes BS, Carvalho FD, Guilhermino LM, Van Stappen G (2006) Use of the genus Artemia in ecotoxicity testing. Environ Pollut 144(2):453–462. https://doi.org/10.1016/j.envpol.2005.12.037

    Article  CAS  PubMed  Google Scholar 

  32. Ntungwe NE, Domínguez-Martín EM, Roberto A, Tavares J, Isca VMS, Pereira P, Cebola M-J, Rijo P (2020) Artemia species: an important tool to screen general toxicity samples. Curr Pharm Des 26(24):2892–2908

    Article  Google Scholar 

  33. Baharom ZS, Ishak MY (2015) Determination of heavy metal accumulation in fish species in Galas River, Kelantan and Beranang Mining Pool, Selangor. Procedia Environ Sci 30:320–325. https://doi.org/10.1016/j.proenv.2015.10.057

    Article  CAS  Google Scholar 

  34. Baki MA, Hossain MM, Akter J, Quraishi SB, Shojib MFH, Ullah AA, Khan MF (2018) Concentration of heavy metals in seafood (fishes, shrimp, lobster and crabs) and human health assessment in Saint Martin Island, Bangladesh. Ecotoxicol Environ Saf 159:153–163. https://doi.org/10.1016/j.ecoenv.2018.04.035

    Article  CAS  PubMed  Google Scholar 

  35. Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82(1):70–77. https://doi.org/10.1016/0003-9861(59)90090-6

    Article  CAS  PubMed  Google Scholar 

  36. Lowry O, Rosebrough N, Farr A, Randall R (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275

    Article  CAS  PubMed  Google Scholar 

  37. Aebi H (1974) Catalase. In: Bergmeyer HU (ed) Methods of enzymatic analysis, vol 2. Academic Press, New York, pp 673–684

    Chapter  Google Scholar 

  38. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44(1):276–287. https://doi.org/10.1016/0003-2697(71)90370-8

    Article  CAS  PubMed  Google Scholar 

  39. Slater TF (1984) Overview of methods used for detecting lipid peroxidation. Methods Enzymol 105:283–293. https://doi.org/10.1016/S0076-6879(84)05036-9

    Article  CAS  PubMed  Google Scholar 

  40. Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24(12):1337–1344. https://doi.org/10.1046/j.1365-3040.2001.00778.x

    Article  CAS  Google Scholar 

  41. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases: the first enzymatic step in mercapturic acid formation. J Biol Chem 249(22):7130–7139. https://doi.org/10.1016/S0021-9258(19)42083-8

    Article  CAS  PubMed  Google Scholar 

  42. Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7(2):88–90. https://doi.org/10.1016/0006-2952(61)90145-9

    Article  CAS  PubMed  Google Scholar 

  43. Devi SS, Sethu M, Lalithambigai P, Priya PG (2017) Study on the effect of Artemia franciscana on the uptake of Zn(II) and Cu(II). J Water Chem Technol 39(1):40–46. https://doi.org/10.3103/S1063455X17010076

    Article  Google Scholar 

  44. Thall A, Acey R (1985) Cadmium binding proteins in developing Artemia. Fed Proc 44(5):1461

    Google Scholar 

  45. Rafiee P, Matthews CO, Bagshaw JC, MacRae TH (1986) Reversible arrest of Artemia development by cadmium. Can J Zool 64(8):1633–1641. https://doi.org/10.1139/z86-246

    Article  CAS  Google Scholar 

  46. Mohiseni M, Farhangi M, Agh N, Mirvaghefi A, Talebi K (2017) Toxicity and bioconcentration of cadmium and copper in Artemia urmiana nauplii. Iran J Toxicol 11(1):33–41

    Article  CAS  Google Scholar 

  47. Mohamed AH, Sheir SK, Osman GY, Abd-El Azeem HH (2014) Toxic effects of heavy metals pollution on biochemical activities of the adult brine shrimp, Artemia salina. Can J Pure Appl Sci 8(3):3019–3028

    Google Scholar 

  48. Trinchella F, Riggio M, Filosa S, Volpe MG, Parisi E, Scudiero R (2006) Cadmium distribution and metallothionein expression in lizard tissues following acute and chronic cadmium intoxication. Comp Biochem Physiol C Toxicol Pharmacol 144(3):272–278. https://doi.org/10.1016/j.cbpc.2006.09.004

    Article  CAS  PubMed  Google Scholar 

  49. Acey RA, Yoshida BN, Edep ME (1989) Metalloproteins in developing Artemia. In: Warner AH, MacRae TH, Bagshaw JC (eds) Cell and molecular biology of Artemia development. Plenum Press, New York, pp 203–219

    Chapter  Google Scholar 

  50. Barata C, Markich SJ, Baird DJ, Taylor G, Soares AMVM (2002) Genetic variability in sublethal tolerance to mixtures of cadmium and zinc in clones of Daphnia magna Straus. Aquat Toxicol 60(1–2):85–99. https://doi.org/10.1016/S0166-445X(01)00275-2

    Article  CAS  PubMed  Google Scholar 

  51. Tamás MJ, Sharma SK, Ibstedt S, Jacobson T, Christen P (2014) Heavy metals and metalloids as a cause for protein misfolding and aggregation. Biomolecules 4(1):252–267. https://doi.org/10.3390/biom4010252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Sarabia R, Del Ramo J, Varo I, Diaz-Mayans J, Torreblanca A (2002) Comparing the acute response to cadmium toxicity of nauplii from different populations of Artemia. Environ Toxicol Chem 21(2):437–444. https://doi.org/10.1002/etc.5620210229

    Article  CAS  PubMed  Google Scholar 

  53. Sandrini JZ, Regoli F, Fattorini D, Notti A, Inácio AF, Linde-Arias AR, Laurino J, Bainy ACD, Marins LFF, Monserrat JM (2006) Short-term responses to cadmium exposure in the estuarine polychaete Laeonereis acuta (Polychaeta, Nereididae): subcellular distribution and oxidative stress generation. Environ Toxicol Chem 25(5):1337–1344. https://doi.org/10.1897/05-275R.1

    Article  CAS  PubMed  Google Scholar 

  54. Pacheco GKÑ, Maldonado NSS, Alta RYP, Vitorino HA (2021) Short exposure of Artemia salina to group-12 metals: comparing hatchability, mortality, lipid peroxidation, and swimming speed. Ecotoxicol Environ Saf 213:112052. https://doi.org/10.1016/j.ecoenv.2021.112052

    Article  CAS  Google Scholar 

  55. Ates M, Daniels J, Arslan Z, Farah IO, Rivera HF (2013) Comparative evaluation of impact of Zn and ZnO nanoparticles on brine shrimp (Artemia salina) larvae: effects of particle size and solubility on toxicity. Environ Sci Process Impacts 15(1):225–233. https://doi.org/10.1039/C2EM30540B

    Article  CAS  PubMed  Google Scholar 

  56. Wang J, Zhu X, Huang X, Gu L, Chen Y, Yang Z (2016) Combined effects of cadmium and salinity on juvenile Takifugu obscurus: cadmium moderates salinity tolerance; salinity decreases the toxicity of cadmium. Sci Rep 6:30968. https://doi.org/10.1038/srep30968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Ortega P, Vitorino HA, Moreira RG, Pinheiro MAA, Almeida AA, Custódio MR, Zanotto FP (2017) Physiological differences in the crab Ucides cordatus from two populations inhabiting mangroves with different levels of cadmium contamination. Environ Toxicol Chem 36(2):361–371. https://doi.org/10.1002/etc.3537

    Article  CAS  PubMed  Google Scholar 

  58. Jiang Q-C, Dilixiati A, Zhang C, Liu X-Z, Huang W-T, Lv L-L, Wang Q, Yang J-X (2013) Metabolic and antioxidant responses in juveniles of Cherax quadricarinatus under acute cadmium stress. J Crustac Biol 33(4):552–556. https://doi.org/10.1163/1937240X-00002149

    Article  Google Scholar 

  59. Wang M-H, Wang G-Z (2009) Biochemical response of the copepod Tigriopus japonicus Mori experimentally exposed to cadmium. Arch Environ Contam Toxicol 57:707–717. https://doi.org/10.1007/s00244-009-9319-6

    Article  CAS  PubMed  Google Scholar 

  60. Pirsaheb M, Azadi NA, Miglietta ML, Sayadi MH, Blahova J, Fathi M, Mansouri B (2019) Toxicological effects of transition metal-doped titanium dioxide nanoparticles on goldfish (Carassius auratus) and common carp (Cyprinus carpio). Chemosphere 215:904–915. https://doi.org/10.1016/j.chemosphere.2018.10.111

    Article  CAS  PubMed  Google Scholar 

  61. Jemec A, Drobne D, Tišler T, Trebše P, Roš M, Sepčić K (2007) The applicability of acetylcholinesterase and glutathione S-transferase in Daphnia magna toxicity test. Comp Biochem Physiol C Toxicol Pharmacol 144(4):303–309. https://doi.org/10.1016/j.cbpc.2006.10.002

    Article  CAS  PubMed  Google Scholar 

  62. Nunes B, Carvalho F, Guilhermino L (2006) Effects of widely used pharmaceuticals and a detergent on oxidative stress biomarkers of the crustacean Artemia parthenogenetica. Chemosphere 62(4):581–594. https://doi.org/10.1016/j.chemosphere.2005.06.013

    Article  CAS  PubMed  Google Scholar 

  63. Najimi S, Bouhaimi A, Daubèze M, Zekhnini A, Pellerin J, Narbonne JF, Moukrim A (1997) Use of acetylcholinesterase in Perna perna and Mytilus galloprovincialis as a biomarker of pollution in Agadir Marine Bay (South of Morocco). Bull Environ Contam Toxicol 58(6):901–908. https://doi.org/10.1007/s001289900419

    Article  CAS  PubMed  Google Scholar 

  64. Gagné F, Cejka P, André C, Hausler R, Blaise C (2007) Neurotoxicological effects of a primary and ozonated treated wastewater on freshwater mussels exposed to an experimental flow-through system. Comp Biochem Physiol C Toxicol Pharmacol 146(4):460–470. https://doi.org/10.1016/j.cbpc.2007.04.006

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

Biljana Kukavica: conceptualization, methodology, validation, formal analysis, ınvestigation, data curation, writing — original draft. Biljana Davidović-Plavšić: conceptualization, methodology, validation, formal analysis, ınvestigation, data curation, review and correction. Ana Savić: data curation, review and correction. Dejan Dmitrović: conceptualization, methodology, review and correction. Goran Šukalo: conceptualization, methodology, review and correction. Sandra Đurić-Savić: formal analysis, data curation. Goran Vučić: formal analysis, data curation. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Biljana Kukavica.

Ethics declarations

Competing interests

The authors declare no competing interests.

Ethics Approval

This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of Medical Faculty University of Banja Luka (No. 18/1.190–18/22).

Consent for Publication

Not applicable.

Conflict of Interest

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.

Supplementary Information

Supplementary Figure 1:

Online Resource 1 Representative native SOD gel of control and treated samples of A. franciscana after 24 and 48 h. The arrow indicates the detected SOD isoform and its Rf value (PNG 482 kb)

High resolution image (TIF 3.63 MB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kukavica, B., Davidović-Plavšić, B., Savić, A. et al. Oxidative Stress and Neurotoxicity of Cadmium and Zinc on Artemia franciscana. Biol Trace Elem Res 201, 2636–2649 (2023). https://doi.org/10.1007/s12011-022-03352-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-022-03352-x

Keywords

Navigation