Skip to main content
Log in

Metals Distribution, Histopathological Alterations, and Health Risk Assessment in Different Tissues of Fish (Ctenopharyngodon idella)

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

Abstract

Grass carps were exposed to the established lethal concentration (LC) values of copper (Cu), chromium (Cr), and lead (Pb) each for the exposed period of 24, 48, 72, and 96 h respectively. Concentrations of these metals were determined in the brain, liver, muscles, gills, kidneys, and intestinal tissues of exposed and control fish through the atomic absorption spectrophotometer after the wet digestion process. The metals accumulation inside these tissues confirmed the absorption of metals from media into the tissues of the model organism. The accumulated concentration in fish tissues was confirmed to be concentration-dependent with significant (p < 0.05) elevated mean values seen for the lead followed by chromium and copper as compared with the mean concentration values of their respective control group. Levels of metals were found above the permissible standards suggested by the regulatory authorities in the fish’s body. Histological sections of the same targeted organs exposed to the three exposure concentration groups were studied and compared with the sections of the healthy group. The histopathological lesions were scored to rank the deleterious effects of metals. The histopathological changes were recorded in concentration and progressive time-related series where gills had the greatest number of scored lesions followed by the kidneys and intestines, muscles, brain, and finally the liver as the least affected organ. Moreover, the organs were not affected uniformly by the metals; in fact, every studied organ has given mild to severe responses towards the toxic metals where lead had proven to cause more severe lesions as compared with copper and chromium. The histological lesions recorded mostly were thus concentration-dependent as revealed in the bioaccumulation of these metals with the effects ranked as lead > chromium > copper with a few exceptions. The findings can be used as a benchmark for the evaluation of the fate and effects of the toxic metals in the expanded aquaculture production of grass carp nationwide. Further investigations with respect to other potentially toxic metals like arsenic, mercury, and cadmium could address the problem towards additional studies.

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.

Institutional subscriptions

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

Similar content being viewed by others

References

  1. Perera P, Kodithuwakku S, Sundarabarathy T, Edirisinghe U (2015) Bioaccumulation of cadmium in freshwater fish: Environ Health Perspect. Insight Ecol 4(1):1–12

  2. Shun-Xing L, Hua-Sheng H, Feng-Ying Z, Nan-Sheng D, Fang L (2007) Influence of nitrate on metal sorption and bioaccumulation in marine phytoplankton, Dunaliella salina. Environ Toxicol 22(6):582–586

    Article  PubMed  CAS  Google Scholar 

  3. Mo N (2016) The effects of bioaccumulation of heavy metals on fish fin over two years. J Fisheries Livest Prod 4:170. https://doi.org/10.4172/2332-2608.1000170

  4. Roberts AP, Oris JT (2004) Multiple biomarker response in rainbow trout during exposure to hexavalent chromium. Comp Biochem Physiol C Toxicol Pharmacol 138(2):221–228. https://doi.org/10.1016/j.cca.2004.08.006

    Article  CAS  PubMed  Google Scholar 

  5. Jakimska A, Konieczka P, Skóra K, Namieśnik J (2011) Bioaccumulation of metals in tissues of marine animals, part I: the role and impact of heavy metals on organisms. Pol J Environ Stud 20(5) 1117–1125 

  6. Coen N, Mothersill C, Kadhim M, Wright E (2001) Heavy metals of relevance to human health induce genomic instability. J Pathol 195(3):293–299

    Article  CAS  PubMed  Google Scholar 

  7. Shah N, Khan A, Habib Khan N, Khisroon M (2020) Genotoxic consequences in common grass carp (Ctenopharyngodon idella Valenciennes, 1844) exposed to selected toxic metals. Biol Trace Elem Res. https://doi.org/10.1007/s12011-020-02122-x

  8. Monteiro DA, Thomaz JM, Rantin FT, Kalinin AL (2013) Cardiorespiratory responses to graded hypoxia in the neotropical fish matrinxã (Brycon amazonicus) and traíra (Hoplias malabaricus) after waterborne or trophic exposure to inorganic mercury. Aquat Toxicol 140:346–355

    Article  PubMed  CAS  Google Scholar 

  9. Bandpei AM, Bay A, Zafarzadeh A, Hassanzadeh V (2016) Bioaccumulation of heavy metals muscle of common carp fish (Cyprinus carpio L, 1758) from Ala gul and Alma gul wetlands of Golestan and consumption risk assessment. Int J Med Res Health Sci 5(11):267–273

    Google Scholar 

  10. Kousar S, Javed M (2014) Heavy metals toxicity and bioaccumulation patterns in the body organs of four fresh water fish species. Pak Vet J 34(2):161–164

    CAS  Google Scholar 

  11. Bernet D, Schmidt H, Meier W, Burkhardt-Holm P, Wahli T (1999) Histopathology in fish: proposal for a protocol to assess aquatic pollution. J Fish Dis 22(1):25–34

    Article  Google Scholar 

  12. Monteiro SM, Mancera JM, Fontaínhas-Fernandes A, Sousa M (2005) Copper induced alterations of biochemical parameters in the gill and plasma of Oreochromis niloticus. Comp Biochem Physiol C Toxicol Pharmacol 141(4):375–383 

  13. Reddy P, Rawat S (2013) Assessment of aquatic pollution using histopathology in fish as a protocol. Int Res J Environ Sci 2(8):79–82

    Google Scholar 

  14. Khoshnood Z, Khodabandeh S, Mosafer S, Khoshnood R (2010) Effects of cortisol on gill chloride cells in Persian sturgeon, Acipenser persicus, fry. Yakhteh Med J (Cell J) 11(4):424–431

  15. Camargo MM, Martinez CB (2007) Histopathology of gills, kidney and liver of a neotropical fish caged in an urban stream. Neotrop. Ichthyol 5(3):327–336

  16. Jortner BS (2005) Neuropathological assessment in acute neurotoxic states. The “dark” neuron. J Med CBR Def 3:1–5

    Google Scholar 

  17. Erhunmwunse N, Ekaye S, Ainerua M, Ewere E (2014) Histopathological changes in the brain tissue of Africa catfish exposure to glyphosate herbicide. J Appl Sci Environ Manag 18(2):275–280

    Google Scholar 

  18. Mela M, Randi M, Ventura D, Carvalho C, Pelletier E, Ribeiro CO (2007) Effects of dietary methylmercury on liver and kidney histology in the neotropical fish Hoplias malabaricus. Ecotoxicol Environ Saf 68(3):426–435

    Article  CAS  PubMed  Google Scholar 

  19. Ahmed M, Aslam Y, Khan W (2011) Absorption and bioaccumulation of water-borne inorganic mercury in the fingerlings of grass carp, Ctenopharyngodon idella. J Anim Plant Sci 21(2):176–181 

  20. APHA (2018) 2020 QUALITY ASSURANCE/QUALITY CONTROL (2017). In: Standard methods for the examination of water and wastewater. Standard methods for the examination of water and wastewater. American Public Health Association. https://doi.org/10.2105/SMWW.2882.015

  21. Khan MI, Zahoor M, Khan A, Gulfam N, Khisroon M (2019) Bioaccumulation of heavy metals and their genotoxic effect on freshwater mussel. Bull Environ Contam Toxicol 102(1):52–58. https://doi.org/10.1007/s00128-018-2492-4

    Article  CAS  PubMed  Google Scholar 

  22. Imanpoor MR, Bagheri T, Hedayati SAA (2010) The anesthetic effects of clove essence in Persian sturgeon, Acipenser persicus. World J Fish Mar Sci 2(1):29–36

  23. Du Preez H, Steyn G (1992) A preliminary investigation of the concentration of selected metals in the tissues and organs of the tigerfish (Hydrocynus vittatus) from the Olifants River, Kruger National Park, South Africa. Water SA 18(2):131–136

    Google Scholar 

  24. Loon JCV (1980) Analytical atomic absorption spectroscopy selected methods. ISBN: 0127140506. Academic Press, New York

    Google Scholar 

  25. Yousafzai AM, Shakoori AR (2006) Bioaccumulation of chromium, nickle, lead, copper and zinc in the skin of tor putitora as an indicator of the presence of heavy metal load in river Kabul, Pakistan. Pak J Zool 38((4)):341–347

    CAS  Google Scholar 

  26. Bell JG, Tocher DR, Farndale BM, McVicar AH, Sargent JR (1999) Effects of essential fatty acid-deficient diets on growth, mortality, tissue histopathology and fatty acid compositions in juvenile turbot (Scophthalmus maximus). Fish Physiol Biochem 20(3):263–277. https://doi.org/10.1023/A:1007743532618

    Article  CAS  Google Scholar 

  27. Mela M, Guiloski I, Doria H, Rabitto I, Da Silva C, Maraschi A, Prodocimo V, Freire C, Randi M, Ribeiro CO (2013) Risks of waterborne copper exposure to a cultivated freshwater Neotropical catfish (Rhamdia quelen). Ecotoxicol Environ Saf 88:108–116

    Article  CAS  PubMed  Google Scholar 

  28. Shackelford C, Long G, Wolf J, Okerberg C, Herbert R (2002) Qualitative and quantitative analysis of nonneoplastic lesions in toxicology studies. Toxicol Pathol 30(1):93–96

    Article  PubMed  Google Scholar 

  29. Khan H, Khan FA, Sadique U, Ahmad S, Hassan ZU (2019) Genotoxic and toxicopathological effect of aflatoxin B1 in grass carp (Ctenopharyngodon idella).Kafkas Univ Vet Fak Derg 25 (6): 841–848 

  30. Shah N, Khan A, Ali R, Marimuthu K, Uddin MN, Rizwan M, Rahman KU, Alam M, Adnan M, Muhammad JSM, Hussain S, Khisroon M (2020) Monitoring bioaccumulation (in gills and muscle tissues), hematology, and Genotoxic alteration in Ctenopharyngodon idella exposed to selected heavy metals. Biomed Res Int 2020:6185231–6185231. https://doi.org/10.1155/2020/6185231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Bhatnagar A, Devi P (2013) Water quality guidelines for the management of pond fish culture. Int J Environ Sci 3(6):1980

    Google Scholar 

  32. Boyd CE (1982) Water quality management for pond fish culture. Elsevier Scientific Publishing Company, Amsterdam, The Netherlands 

  33. Adeosun F, Taiwo I, Alegbeleye W, Oyekanmi F, Odebiyi O (2012) Heavy metals concentrations in Chrysichthys nigrodigitatus in Arakanga Reservoir, Abeokuta, Ogun State, Nigeria

  34. Fawad M, Yousafzai AM, Haseeb A, Rehman HU, jan Afridi A, Akhtar N, Saeed K, Usman K (2017) Acute toxicity and bioaccumulation of chromium in gills, skin and intestine of goldfish (Carassius auratus). J. Entomol. Zool 5(1):568–71

  35. Glover CN, Hogstrand C (2002) In vivo characterisation of intestinal zinc uptake in freshwater rainbow trout. J Exp Biol 205(1):141–150

    Article  CAS  PubMed  Google Scholar 

  36. Oguzie F (2003) Heavy metals in water and sediment of the lower Ikpoba River, Benin City, Nigeria. Pak J Sci Ind Res 46 (3):156–160

  37. Shrivastava P, Saxena A, Swarup A (2003) Heavy metal pollution in a sewage-fed lake of Bhopal,(MP) India. Lakes Reserv Res Manag 8(1):1–4

    Article  CAS  Google Scholar 

  38. Łuszczek-Trojnar E, Drąg-Kozak E, Popek W (2013) Lead accumulation and elimination in tissues of Prussian carp, Carassius gibelio (Bloch, 1782), after long-term dietary exposure, and depuration periods. Environ Sci Pollut Res 20(5):3122–3132

    Article  CAS  Google Scholar 

  39. Ravera O, Cenci R, Beone GM, Dantas M, Lodigiani P (2003) Trace element concentrations in freshwater mussels and macrophytes as related to those in their environment. J Limnol 62(1):61–70

    Article  Google Scholar 

  40. Odongo KO (2017) Morphological effects of selected heavy metals on the Nile tilapia Oreochromis Niloticus and African catfish Clarias gariepinus along River Ruiru. Kenyatta University, Nairobi

    Google Scholar 

  41. Aldoghachi MJ, Rahman MM, Yusoff I, Sofian-Azirun M (2016) Acute toxicity and bioaccumulation of heavy metals in red tilapia fish. J Animal Plant Sci 26(2):507–513 

  42. Kamaruzzaman B, Akbar B, Jalal K, Shahbudin S (2010) Accumulation of metals in the gills of tilapia fingerlings (Oreochromis niloticus) from in vitro toxicology study. J Fish Aquat Sci 5(6):503–509

    Article  CAS  Google Scholar 

  43. Kotze P, Du Preez H, Van Vuren J (1999) Bioaccumulation of copper and zinc in Oreochromis mossambicus and Clarias gariepinus, from the Olifants River, Mpumalanga, South Africa. Water Sa-Pretoria 25:99–110

    CAS  Google Scholar 

  44. Narges AB, Ahmad S, Mohammadsedigh M, Hossein Z, Negin S, Zohreh AB (2012) Non-essential metals (Cd & Pb) accumulation and elimination in liver tissue of juvenile milkfish, after sublethal exposure

  45. WHO (1989) Heavy metals-environmental aspects. Environment Health Criteria., vol 85. Geneva, Switzerland. https://doi.org/10.1016/S0076-6879(84)05016-3

  46. Mokhtar MB, Aris AZ, Munusamy V, Praveena SM (2009) Assessment level of heavy metals in Penaeus monodon and Oreochromis spp. in selected aquaculture ponds of high densities development area. Eur J Sci Res 30(3):348–360

    Google Scholar 

  47. Svobodová Z (1993) Water quality and fish health, EIFAC Technical Paper. No. 54. Rome, FAO, pp. 56–57.

  48. Idriss A, Ahmad A (2015) Heavy metal concentrations in fishes from Juru River, estimation of the health risk. Bull Environ Contam Toxicol 94(2):204–208

    Article  CAS  PubMed  Google Scholar 

  49. Kalay M, Canli M (2000) Elimination of essential (Cu, Zn) and non-essential (Cd, Pb) metals from tissues of a freshwater fish Tilapia zilli. Turk J Zool 24(4):429–436

  50. Fathi H, Othman M, Mazlan A, Arshad A, Amin S, Simon K (2013) Trace metals in muscle, liver and gill tissues of marine fishes from Mersing, eastern coast of peninsular Malaysia: concentration and assessment of human health risk. Asian J Anim Vet Adv 8(2):227–236

  51. Jovanović DA, Marković RV, Teodorović VB, Šefer DS, Krstić MP, Radulović SB, Ivanović Ćirić JS, Janjić JM, Baltić MŽ (2017) Determination of heavy metals in muscle tissue of six fish species with different feeding habits from the Danube River, Belgrade—public health and environmental risk assessment. Environ Sci Pollut Res 24(12):11383–11391. https://doi.org/10.1007/s11356-017-8783-1

    Article  CAS  Google Scholar 

  52. Fernandes C, Fontaínhas-Fernandes A, Cabral D, Salgado MA (2008) Heavy metals in water, sediment and tissues of Liza saliens from Esmoriz–Paramos lagoon, Portugal. Environ Monit Assess 136(1–3):267–275

    CAS  PubMed  Google Scholar 

  53. Svecevičius G (2006) Acute toxicity of hexavalent chromium to European freshwater fish. Bull Environ Contam Toxicol 77(5):741–747

    Article  PubMed  CAS  Google Scholar 

  54. Arunkumar RI, Rajasekaran P, Michael RD (2000) Differential effect of chromium compounds on the immune response of the African mouth breeder Oreochromis mossambicus (Peters). Fish Shellfish Immunol 10(8):667–676

    Article  CAS  PubMed  Google Scholar 

  55. Shah N, Khisroon M, Shah SSA (2020) Assessment of copper, chromium, and lead toxicity in fish (Ctenopharyngodon idella Valenciennes, 1844) through hematological biomarkers. Environ Sci Pollut Res 27:33259–33269. https://doi.org/10.1007/s11356-020-09598-z

    Article  CAS  Google Scholar 

  56. Annabi A, Said K, Messaoudi I (2013) Cadmium: bioaccumulation, histopathology and detoxifying mechanisms in fish. Am J Res Commun 1(4):62

  57. Melgar M, Perez M, Garcia M, Alonso J, Miguez B (1997) The toxic and accumulative effects of short-term exposure to cadmium in rainbow trout (Oncorhynchus mykiss). Vet Hum Toxicol 39(2):79–83

    CAS  PubMed  Google Scholar 

  58. Mansouri B, Baramaki R, Zareh M, Pourkhabbaz A, Hamidian AH (2013) Bioaccumulation and depuration of copper in the kidney and liver of a freshwater fish, Capoeta fusca. Iran J Toxicol 7(20):816–822

  59. Popović M, Nedić D, Pećanac B, Đorđević V, Baltić T, Lazić IB, Ćirić J (2020) The toxic element concentration in fish tissues from Saničani Lake, an urban environment, in Bosnia and Herzegovina. Biol Trace Elem Res 197(1):271–278. https://doi.org/10.1007/s12011-019-01982-2

    Article  CAS  PubMed  Google Scholar 

  60. Ivanović J, Janjić J, Baltić M, Milanov R, Bošković M, Marković RV, Glamočlija N (2016) Metal concentrations in water, sediment and three fish species from the Danube River, Serbia: a cause for environmental concern. Environ Sci Pollut Res 23(17):17105–17112. https://doi.org/10.1007/s11356-016-6875-y

    Article  CAS  Google Scholar 

  61. Mahboob S, Kausar S, Jabeen F, Sultana S, Sultana T, Al-Ghanim K, Hussain B, Al-Misned F, Ahmed Z (2016) Effect of heavy metals on liver, kidney, gills and muscles of Cyprinus carpio and Wallago attu inhabited in the Indus. Braz Arch Biol Technol 59

  62. Opaluwa O, Aremu M, LOGBO L, Imagaji J, EOdiba I (2012) Assessment of heavy metals in water, fish and sediments from UKE stream, Nasarawa State, Nigeria. Curr World Environ 7(2):213–220

    Article  CAS  Google Scholar 

  63. Malakootian M, Mortazavi MS, Ahmadi A (2016) Heavy metals bioaccumulation in fish of southern Iran and risk assessment of fish consumption. Environ Health Eng Manag 3(2):61–68

  64. Öztürk M, Özözen G, Minareci O, Minareci E (2009) Determination of heavy metals in fish, water and sediments of Avsar Dam Lake in Turkey. J Environ Health Sci Eng 6(2):73–80

    Google Scholar 

  65. Commission E (2005) Commission Regulation (EC) No. 78/2005 of 19 January 2005, amending Regulation (EC) No. 466/2001 as regards heavy metals. Off J Eur Union 16

  66. Ikem A, Egiebor NO (2005) Assessment of trace elements in canned fishes (mackerel, tuna, salmon, sardines and herrings) marketed in Georgia and Alabama (United States of America). J Food Compos Anal 18(8):771–787

    Article  CAS  Google Scholar 

  67. Obasohan E (2007) Heavy metals concentrations in the offal, gill, muscle and liver of a freshwater mudfish (Parachanna obscura) from Ogba River, Benin city, Nigeria. Afr J Biotechnol 6(22):2620–2627

    Article  CAS  Google Scholar 

  68. Ahmad Z (2014) Biomonitoring of heavy metal in selected biomarkers of Clarias gariepinus (Burchell, 1822), a comparative study of river Galma, river Kubani and fish farms in Zaria, Nigeria. Adv Appl Sci Res 5(6):198–206

    Google Scholar 

  69. Adeyemo OK (2008) Histological alterations observed in the gills and ovaries of Clarias gariepinus exposed to environmentally relevant lead concentrations. JSTOR

  70. Sorensen EM (1991) Metal poisoning in fish: Environmental and Life Sciences Associates. Boca Raton: CRC Press Inc. 

  71. Nordberg GF, Fowler BA, Nordberg M (2014) Handbook on the Toxicology of Metals. Fourth. Academic Press; 2015. p 461–86

  72. Aslam S, Yousafzai AM (2017) Chromium toxicity in fish: a review article. J. Entomol 5(3):1483–1488

  73. Kumari K, Ranjan N, Sinha R (2011) Multiple biomarker response in the fish, Labeo rohita due to hexavalent chromium. In: Proceedings of the 2nd international conference on biotechnology and food science (IPCBEE’11), IACSIT Press,

  74. Shafiq-ur-Rehman (2003) Lead-exposed increase in movement behavior and brain lipid peroxidation in fish. J Environ Sci Health A 38(4):631–643

    Article  CAS  Google Scholar 

  75. Łuszczek-Trojnar E, Drąg-Kozak E, Szczerbik P, Socha M, Popek W (2014) Effect of long-term dietary lead exposure on some maturation and reproductive parameters of a female Prussian carp (Carassius gibelio B.). Environ Sci Pollut Res 21(4):2465–2478

    Article  CAS  Google Scholar 

  76. Rocha E. & Monteiro R.A.F (1999) Histology and cytology of fish liver: A review, p.321-344. In: Saksena D.N. (ed.) Ichthyology: Recent research advances. Science Publishers, Enfield, New Hampshire

  77. Al-Yousuf M, El-Shahawi M, Al-Ghais S (2000) Trace metals in liver, skin and muscle of Lethrinus lentjan fish species in relation to body length and sex. Sci Total Environ 256(2–3):87–94

    Article  CAS  PubMed  Google Scholar 

  78. Das BK, Mukherjee SC (2000) A histopathological study of carp (Labeo rohita) exposed to hexachlorocyclohexane. Vet Arh 70(4):169–180 

  79. Susan TA, Sobha K, Tilak K (2012) Toxicity and histopathological changes in the three Indian major carps, Labeo rohita (Hamilton), Catla catla (Hamilton) and Cirrhinus mrigala (Hamilton) exposed to fenvalerate. Int J Plant Anim and Environ Sci 2(1):18–32 

  80. Thophon S, Kruatrachue M, Upatham E, Pokethitiyook P, Sahaphong S, Jaritkhuan S (2003) Histopathological alterations of white seabass, Lates calcarifer, in acute and subchronic cadmium exposure. Environ Pollut 121(3):307–320

    Article  CAS  PubMed  Google Scholar 

  81. Burlinson B, Tice RR, Speit G, Agurell E, Brendler-Schwaab SY, Collins AR, Escobar P, Honma M, Kumaravel TS, Nakajima M (2007) Fourth international workgroup on genotoxicity testing: results of the in vivo comet assay workgroup. Mutat Res Genet Toxicol Environ Mutagen 627(1):31–35

    Article  CAS  Google Scholar 

  82. Jones T, Hunt R, King N (1997) The digestive system: peritoneum. Veterinary Pathology, 6th edn. Williams & Wilkins, Baltimore, pp 1087–1089

    Book  Google Scholar 

  83. Vasquez MZ (2009) Combining the in vivo comet and micronucleus assays: a practical approach to genotoxicity testing and data interpretation. Mutagenesis 25(2):187–199

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  84. AnvariFar H, Amirkolaie AK, Jalali AM, Miandare HK, Sayed AH, Üçüncü Sİ, Ouraji H, Ceci M, Romano N (2018) Environmental pollution and toxic substances: cellular apoptosis as a key parameter in a sensible model like fish. Aquat Toxicol 204:144–159. https://doi.org/10.1016/j.aquatox.2018.09.010

    Article  CAS  PubMed  Google Scholar 

  85. Madkour LH (2018) Toxic effects of environmental heavy metals on cardiovascular pathophysiology and heart health function: chelation therapeutics. UPI J Pharma Med Health Sci (UPI-JPMHS) 1(1):19–62

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nazish Shah.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval

Ethical approval for the study was taken from the Ethical Committee, University of Peshawar.

Additional information

Publisher’s Note

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

Electronic Supplementary Material

ESM 1

(DOCX 31279 kb).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shah, N., Khisroon, M. & Shah, S.S.A. Metals Distribution, Histopathological Alterations, and Health Risk Assessment in Different Tissues of Fish (Ctenopharyngodon idella). Biol Trace Elem Res 199, 2730–2752 (2021). https://doi.org/10.1007/s12011-020-02373-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-020-02373-8

Keywords

Navigation