Advertisement

The impacts of individual and combined exposure to cadmium and lead on intraocular pressure, electroretinography, and residual changes in the rabbit eyes

  • Yasmina M. Abd-ElhakimEmail author
  • Khlood M. El Bohi
  • Nabela I. El Sharkawy
  • Manar A. Ghali
  • Sarah Haseeb
Research Article
  • 11 Downloads

Abstract

The human eye is very vulnerable to various environmental pollutants. Cadmium (Cd) and lead (Pb) are widely spread heavy metals. The goal of the existing study is to explore the impact of single or joint exposure to Cd and Pb on the eye indicators. In this study, male New Zealand white rabbits were treated orally for 30 days with Cd (5 mg Cd Cl2/kg bw) associated or not with Pb (12.5 mg lead acetate/kg bw). Fundus and slit lamp examinations, electroretinography (ERG), intraocular pressure (IOP), Cd and Pb residues, and the histopathological picture of the eye were studied. The results revealed that the oral dosing of Cd or Pb evoked a significant (p < 0.05) decline in a- and b-wave amplitudes, under scotopic conditions, and IOP values. Single Pb or Cd treatment showed a significant (p < 0.001) increase in their residues in the whole eye tissue of the Pb- or Cd-treated group. Eye structures of Cd- or Pb-intoxicated rabbit showed mild degenerated changes of cornea and sclera tissues with the presence of irregular variably sized eosinophilic droplets in the lens. Notably, the simultaneous exposure to Cd and Pb leads to an antagonistic outcome in all of the estimated parameters. These findings concluded that oral exposure to Cd or Pb could significantly disturb the vision but their joint exposure caused an opposing effect on nearly all of these disturbances.

Keywords

Cadmium Lead Toxicity Eye Rabbit Electroretinography Applanation tonometry 

Notes

Acknowledgments

The authors are grateful to Prof. Dr. Sayed Rashad El-Attar, Professor of Pathology, Faculty of Veterinary Medicine, Zagazig University, for his support in histopathological studies.

Compliance with ethical standards

Conflict of interests

The authors declare that they have no conflict of interests.

Statement of ethical approval

The Ethics of Animal Use in Research Committee (EAURC) of the university permitted all protocols comprising animals here. All experimental procedures were conducted following the Directive 2010/63/EU of the European Parliament and of the Council of September 22, 2010, on the protection of animals used for scientific aims.

References

  1. Abd-Elhakim YM, El Sharkawy NI, El Bohy KM, Gomaa M, Haseeb S (2017) Morphological, biochemical, and histopathological postmortem ocular indices following subchronic exposure to cadmium and/or lead in a rabbit model. Environ Sci Pollut Res:1–14Google Scholar
  2. Adamse P, Van der Fels-Klerx H, de Jong J (2017) Cadmium, lead, mercury and arsenic in animal feed and feed materials–trend analysis of monitoring results. Food Addit Contam Part A 34:1298–1311CrossRefGoogle Scholar
  3. Al Amry M, Al-Saikhan F, Ayoubi A (2011) Toxic effect of cadmium found in eyeliner to the eye of a 21 year old Saudi woman: a case report. Saudi Pharm J 19:269–272CrossRefGoogle Scholar
  4. Andjelkovic M et al (2019) Toxic effect of acute cadmium and lead exposure in rat blood, liver, and kidney. Int J Environ Res Public Health 16:274.  https://doi.org/10.3390/ijerph16020274 CrossRefGoogle Scholar
  5. Asagba SO (2010) A comparative study on the biochemical effect of ocular and oral cadmium administration in rabbits. Afr J Biotechnol 9:3016–3025Google Scholar
  6. Bancroft JD, Floyd AD, Suvarna SK (2013) Bancroft’s theory and practice of histological techniquesGoogle Scholar
  7. Bertin G, Averbeck D (2006) Cadmium: cellular effects, modifications of biomolecules, modulation of DNA repair and genotoxic consequences (a review). Biochimie 88:1549–1559CrossRefGoogle Scholar
  8. Bressler JP, Olivi L, Cheong JH, Kim Y, Bannona D (2004) Divalent metal transporter 1 in lead and cadmium transport. Ann N Y Acad Sci 1012:142–152CrossRefGoogle Scholar
  9. Colasanti BK, Craig CR, Allara RD (1984) Intraocular pressure, ocular toxicity and neurotoxicity after administration of cannabinol or cannabigerol. Exp Eye Res 39:251–259CrossRefGoogle Scholar
  10. De Letter E, De Paepe P, Clauwaert K, Belpaire F, Lambert W, Van Bocxlaer J, Piette M (2000) Is vitreous humour useful for the interpretation of 3, 4-methylenedioxymethamphetamine (MDMA) blood levels? Int J Legal Med 114:29–35CrossRefGoogle Scholar
  11. DECOS (1991) (Dutch Expert Committee for Occupational Standards) Ethyl acetate. Health based recommended occupational exposure limit, RA 10/91, Sdu Uitgeverij, Den HaagGoogle Scholar
  12. Denniston A, Murray P (2014) Oxford handbook of ophthalmology. OUP, OxfordCrossRefGoogle Scholar
  13. Ekİncİ D, Beydemir Ş, Küfrevİoğlu Öİ (2007) In vitro inhibitory effects of some heavy metals on human erythrocyte carbonic anhydrases. J Enzyme Inhib Med Chem 22:745–750CrossRefGoogle Scholar
  14. Elgohary A, Shafaa M, Raafat B, Rizk R, Metwally F, Saleh A (2009) Prophylactic effect of Angelica archangelica against acute lead toxicity in albino rabbits. Rom J Biophys 19:256–275Google Scholar
  15. Erie JC, Butz JA, Good JA, Erie EA, Burritt MF, Cameron JD (2005) Heavy metal concentrations in human eyes. Am J Ophthalmol 139:888–893CrossRefGoogle Scholar
  16. Fox D, Campbell M, Blocker Y (1996) Functional alterations and apoptotic cell death in the retina following developmental or adult lead exposure. Neurotoxicology 18:645–664Google Scholar
  17. Garcia TA, Corredor L (2004) Biochemical changes in the kidneys after perinatal intoxication with lead and/or cadmium and their antagonistic effects when coadministered. Ecotoxicol Environ Saf 57:184–189CrossRefGoogle Scholar
  18. Gjörloff K, Andréasson S, Ehinger B (2004) Standardized full-field electroretinography in rabbits. Doc Ophthalmol 109:163–168CrossRefGoogle Scholar
  19. Goyer RA (1990) Lead toxicity: from overt to subclinical to subtle health effects. Environ Health Perspect 86:177CrossRefGoogle Scholar
  20. Hohberger B et al (2018) Levels of aqueous humor trace elements in patients with open-angle glaucoma. J Trace Elem Med Biol 45:150–155CrossRefGoogle Scholar
  21. Hormozi M, Mirzaei R, Nakhaee A, Izadi S, Dehghan Haghighi J (2018) The biochemical effects of occupational exposure to lead and cadmium on markers of oxidative stress and antioxidant enzymes activity in the blood of glazers in tile industry. Toxicol Ind Health 34:459–467CrossRefGoogle Scholar
  22. Imbrasienė D, Jankauskienė J, Švedienė L (2007) Character of ocular changes in a zone polluted by heavy metals. Ekologija 53:7–10Google Scholar
  23. Kalariya NM, Wills NK, Ramana KV, Srivastava SK, van Kuijk FJ (2009) Cadmium-induced apoptotic death of human retinal pigment epithelial cells is mediated by MAPK pathway. Exp Eye Res 89:494–502CrossRefGoogle Scholar
  24. Lee SH et al (2016) Three toxic heavy metals in open-angle glaucoma with low-teen and high-teen intraocular pressure: a cross-sectional study from South Korea. PLoS One 11:e0164983.  https://doi.org/10.1371/journal.pone.0164983 CrossRefGoogle Scholar
  25. Lei B, Perlman I (1999) The contributions of voltage-and time-dependent potassium conductances to the electroretinogram in rabbits. Vis Neurosci 16:743–754CrossRefGoogle Scholar
  26. Maren TH (1992) Role of carbonic anhydrase in aqueous humour and cerebrospinal fluid formation. In: Segal MB (ed) Barriers and fluids of the eye and brain. Macmillan Education, London, pp 37–48.  https://doi.org/10.1007/978-1-349-12306-3_5 CrossRefGoogle Scholar
  27. Markiewicz-Górka I, Januszewska L, Michalak A, Prokopowicz A, Januszewska E, Pawlas N, Pawlas K (2015) Effects of chronic exposure to lead, cadmium, and manganese mixtures on oxidative stress in rat liver and heart/Utjecaj kronične istodobne izloženosti olovu, kadmiju i manganu na oksidativni stres u jetri i srcu štakora. Arch Ind Hyg Toxicol 66:51–62Google Scholar
  28. Massó EL, Corredor L, Antonio MT (2007) Oxidative damage in liver after perinatal intoxication with lead and/or cadmium. J Trace Elem Med Biol 21:210–216CrossRefGoogle Scholar
  29. McCulloch DL, Marmor MF, Brigell MG, Hamilton R, Holder GE, Tzekov R, Bach M (2015) ISCEV Standard for full-field clinical electroretinography (2015 update). Doc Ophthalmol 130:1–12.  https://doi.org/10.1007/s10633-014-9473-7 CrossRefGoogle Scholar
  30. Mitchell N (2008) Enucleation in companion animals. Ir Vet J 61:108Google Scholar
  31. Mohamed WA, Abd-Elhakim YM, Farouk SM (2016) Protective effects of ethanolic extract of rosemary against lead-induced hepato-renal damage in rabbits. Exp Toxicol Pathol 68:451–461CrossRefGoogle Scholar
  32. Mulak M (1997) The effect of heavy metals (lead, cadmium, and manganese) on the function of the visual system. Med Pr 49:603–607Google Scholar
  33. Mulak M, Misiuk-Hojło M, Markuszewski B, Dembska K (2007) Influence of chronic exposure to heavy metals on eyesight. Klin Ocz 110:176–182Google Scholar
  34. Nampoothiri LP, Agarwal A, Gupta S (2007) Effect of co-exposure to lead and cadmium on antioxidant status in rat ovarian granulose cells. Arch Toxicol 81:145–150CrossRefGoogle Scholar
  35. Nation JR, Grover CA, Bratton GR, Salinas JA (1990) Behavioral antagonism between lead and cadmium. Neurotoxicol Teratol 12:99–104CrossRefGoogle Scholar
  36. Ofri R (2002) Clinical electrophysiology in veterinary ophthalmology–the past, present and future. Doc Ophthalmol 104:5–16CrossRefGoogle Scholar
  37. Ojimogho ES, Odjimogho SE, Eriyamremu GE, Aguebor-Ogie B (2010) Changes in ocular tissue lipid peroxidation and antioxidant enzymes of rabbits fed a wholly compounded Nigerian diet containing excess cadmium levelsGoogle Scholar
  38. Pillai A, Gupta S (2005) Effect of gestational and lactational exposure to lead and/or cadmium on reproductive performance and hepatic oestradiol metabolising enzymes. Toxicol Lett 155:179–186CrossRefGoogle Scholar
  39. Pillai A, Priya PL, Gupta S (2002a) Effects of combined exposure to lead and cadmium on pituitary membrane of female rats. Arch Toxicol 76:671–675CrossRefGoogle Scholar
  40. Pillai A, Rawal A, Gupta S (2002b) Effect of low level exposure of lead and cadmium on hepatic estradiol metabolism in female rats. Indian J Exp Biol 40:807–811Google Scholar
  41. Raafat BM, Shafaa MW, Rizk RA, Elgohary AA, Saleh A (2009) Ameliorating effects of vitamin C against acute lead toxicity in albino rabbits. Aust J Basic Appl Sci 3:3597–3608Google Scholar
  42. Rajaganapathy V, Xavier F, Sreekumar D, Mandal P (2011) Heavy metal contamination in soil, water and fodder and their presence in livestock and products: a review. J Environ Sci Technol 4:234–249CrossRefGoogle Scholar
  43. Richardson ME, Fox MS (1974) Dietary cadmium and enteropathy in the Japanese quail: histochemical and ultrastructural studies. Lab Invest;(United States) 31Google Scholar
  44. Rosen JF, Chesney RW, Hamstra A, DeLuca HF, Mahaffey KR (1980) Reduction in 1, 25-dihydroxyvitamin D in children with increased lead absorption. N Engl J Med 302:1128–1131CrossRefGoogle Scholar
  45. Rouabhi R, Hanene B, Khaled B, Houria B, MohamedReda D (2013) Opposite effects of Ca2+ on toxicity by CdCl2 on white blood cells (WBC), protein level and LD50 of rabbits Oryctolagus cuniculus. J Toxicol Environ Health Sci 5:37–42CrossRefGoogle Scholar
  46. Ruan D-Y, Tang L-X, Zhao C, Guo Y-J (1994) Effects of low-level lead on retinal ganglion sustained and transient cells in developing rats. Neurotoxicol Teratol 16:47–53CrossRefGoogle Scholar
  47. Saccà SC, Pascotto A, Camicione P, Capris P, Izzotti A (2005) Oxidative DNA damage in the human trabecular meshwork: clinical correlation in patients with primary open-angle glaucoma. Arch Ophthalmol 123:458–463CrossRefGoogle Scholar
  48. Saxena R, Srivastava S, Trivedi D, Anand E, Joshi S, Gupta SK (2003) Impact of environmental pollution on the eye. Acta Ophthalmol Scand 81:491–494CrossRefGoogle Scholar
  49. Simons T (1992) Lead-calcium interactions in cellular lead toxicity. Neurotoxicology 14:77–85Google Scholar
  50. Smith E, Gancarz D, Rofe A, Kempson IM, Weber J, Juhasz AL (2012) Antagonistic effects of cadmium on lead accumulation in pregnant and non-pregnant mice. J Hazard Mater 199:453–456CrossRefGoogle Scholar
  51. Soussi A, Gargouri M, El Feki A (2018) Effects of co-exposure to lead and zinc on redox status, kidney variables, and histopathology in adult albino rats. Toxicol Ind Health 34:469–480CrossRefGoogle Scholar
  52. Tempelman DCG, Steerneman AGM (2004) Imputation for economic data under linear restrictions. Statistics NetherlandsGoogle Scholar
  53. Vitale A, Monserrat J, Castilho P, Rodriguez E (1999) Inhibitory effects of cadmium on carbonic anhydrase activity and ionic regulation of the estuarine crab Chasmagnathus granulata (Decapoda, Grapsidae). Comp Biochem Physiol C: Pharmacol Toxicol Endocrinol 122:121–129Google Scholar
  54. Wang X, Dong J, Wu Q (2013) Twenty-four-hour measurement of IOP in rabbits using rebound tonometer. Vet Ophthalmol 16:423–428CrossRefGoogle Scholar
  55. Wang W, Schaumberg DA, Park SK (2016) Cadmium and lead exposure and risk of cataract surgery in US adults Int J Hyg Environ HealthGoogle Scholar
  56. Wilhelmus KR (2001) The Draize eye test. Surv Ophthalmol 45:493–515CrossRefGoogle Scholar
  57. Wilson SL, Ahearne M, Hopkinson A (2015) An overview of current techniques for ocular toxicity testing. Toxicology 327:32–46CrossRefGoogle Scholar
  58. Wu Q, Pierce W Jr, Delamere NA (1998) Cytoplasmic pH responses to carbonic anhydrase inhibitors in cultured rabbit nonpigmented ciliary epithelium. J Membr Biol 162:31–38CrossRefGoogle Scholar
  59. Zhai Q, Narbad A, Chen W (2015) Dietary strategies for the treatment of cadmium and lead toxicity. Nutrients 7:552–571CrossRefGoogle Scholar
  60. Zhang Y-M, Xue-Zhong L, Hao L, Li M, Zong-Ping L (2009) Lipid peroxidation and ultrastructural modifications in brain after perinatal exposure to lead and/or cadmium in rat pups. Biomed Environ Sci 22:423–429CrossRefGoogle Scholar
  61. Zhang J, Ding T-T, Dong X-Q, Bian Z-Q (2018) Time-dependent and Pb-dependent antagonism and synergism towards Vibrio qinghaiensis sp.-Q67 within heavy metal mixtures. RSC Adv 8:26089–26098CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Forensic Medicine and Toxicology, Faculty of Veterinary MedicineZagazig UniversityZagazigEgypt
  2. 2.Ophthalmology Department, Faculty of MedicineZagazig UniversityZagazigEgypt

Personalised recommendations