Skip to main content

Advertisement

Log in

Genotoxic and cytotoxic assessment of individual and composite mixture of cadmium, lead and manganese in Clarias gariepinus (Burchell 1822) using micronucleus assay

  • Original Article
  • Published:
The Nucleus Aims and scope Submit manuscript

Abstract

Heavy metals are ubiquitous environmental and occupational genotoxicants with different absorbability and toxicokinetics towards increasing genetic damage, neoplasm and cell death. Aquatic organisms are exposed to individuals and/or mixtures of these metals. This study investigated the potentials for cadmium(II) (Cd), lead(II) (Pb), manganese(II) (Mn), and their mixture (CPM) to induce cytogenotoxicity in Clarias gariepinus (Family: Clariidae). Clarias gariepinus was exposed to six concentrations ranging from 0 to 1600 mg/L, selected from range finding tests, to evaluate the 96 h acute toxicity for the individual metals and CPM. Fish were exposed to sub-lethal concentrations (6.25, 12.5 25, 50, and 100% of the 96 h LC50) of each metal and their mixture for 7 days to investigate micronucleus (MN) and abnormal nuclei (NAs) in the peripheral blood erythrocytes. Fish were exposed to borehole tap water and 0.01 mL/L of Benzene as negative and positive controls respectively. The tested metals induced toxicity in the order CMP > Cd > Pb > Mn, with CPM (LC50 = 40.6 mg/L) being 11.5 times more toxic than Mn (LC50 = 478.2 mg/L), the least toxic metal, to juvenile catfish. All the tested metals induced significant increase in frequencies of MN and NAs. The induced MN and NAs were in the order CMP > Cd > Mn > Pb. Fragmented and necrotic cells were common NAs in fish treated with 50 and 100% of Cd and CPM, suggesting that severely damaged cells were eliminated by programmed cell death (apoptosis) and/or accidental cell death (necrosis). Antagonistic interaction among the composite mixture of CPM provoked greater genomic instability and cytotoxicity in fish. Significant increase in MN and NAs in exposed fish suggest increased genomic instability which may lead to increase health defects including neoplasms and genetic related disorders, cell dysfunction and/or cell death.

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

Similar content being viewed by others

References

  1. Abdullah S, Javed M, Javid A. Studies on acute toxicity of metals to the fish (Labeo rohita). Int J Agric Biol. 2007;9(2):333–7.

    CAS  Google Scholar 

  2. Alcala-Orozco M, Morillo-Garcia Y, Caballero-Gallardo K, Olivero-Verbe J. Mercury in canned tuna marketed in Cartagena, Colombia, and estimation of human exposure. Food Addit Contam Part B. 2017;10(4):241–7.

    CAS  Google Scholar 

  3. Alimba CG, Adekoya KO, Soyinka OO. Exposure to effluent from pharmaceutical industry induced cytogenotoxicity, hematological and histopathological alterations in Clarias gariepinus (Burchell, 1822). EXCLI J. 2019;18:63–78.

    PubMed  PubMed Central  Google Scholar 

  4. Alimba CG, Ajayi EO, Hassan T, Sowunmi AA, Bakare AA. Cytogenotoxicity of abattoir effluent in Clarias gariepinus (Burchell, 1822) using micronucleus test. Chin J Biol. 1822;2015:1–6. https://doi.org/10.1155/2015/624524.

    Google Scholar 

  5. Alimba CG, Ajiboye RD, Fagbenro OS. Dietary ascorbic acid reduced micronucleus and nuclear abnormalities in Clarias gariepinus (Burchell 1822) exposed to hospital effluent. Fish Physiol Biochem. 2017;43(5):1325–35.

    CAS  PubMed  Google Scholar 

  6. Alimba CG, Aladeyelu AM, Nwabisi IA, Bakare AA. Micronucleus cytome assay in the differential assessment of cytotoxicity and genotoxicity of cadmium and lead in Amietophrynus regularis. EXCLI J. 2018;17:89–101.

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Alimba CG, Bakare AA. In vivo micronucleus test in the assessment of cytogenotoxicity of landfill leachates in three animal models from various ecological habitats. Ecotoxicology. 2016;25:310–9.

    CAS  PubMed  Google Scholar 

  8. Alimba CG, Dhillon V, Bakare AA, Fenech M. Genotoxicity and cytotoxicity of chromium, copper, manganese and lead, and their mixture in WIL2-NS human B lymphoblastoid cells is enhanced by folate depletion. Mutat Res. 2016;798–9:35–47.

    Google Scholar 

  9. Alimba CG, Saliu JK, Ubani-Rex OA. Cytogenotoxicity and histopathological assessment of Lekki Lagoon and Ogun River in Synodontis clarias (Linnaeus, 1758). Toxicol Environ Chem. 2015;97(2):221–34.

    CAS  Google Scholar 

  10. Al-Sabti K, Metcalfe CD. Fish micronuclei for assessing genotoxicity in water. Mutat Res. 1995;343:121–35.

    CAS  PubMed  Google Scholar 

  11. Anderson PD, Weber LJ (1975) The toxicity to aquatic population of mixtures containing certain heavy metals. In: Proceeding of the international conference on heavy metal in the environment. Institute of Environmental Studies, University of Toronto, pp. 933–953

  12. ATSDR (Agency for Toxic Substances and Disease Registry) (1997) CERCLA priority list of hazardous substances that will be the subjects of toxicological profiles and support document, U.S. Department of Health and Human Services

  13. ATSDR (Agency for Toxic Substances and Disease Registry) (1998) Toxicological profile for lead, US Department of Health and Human Services, Atlanta, GA

  14. Bahari IB, Noor FM, Daud NM. Micronucleated erythrocytes as an assay to assess actions by physical and chemical genotoxic agents in Clarias gariepinus. Mutat Res. 1994;313:1–5.

    CAS  PubMed  Google Scholar 

  15. Bawa-Allah KA, Saliu JK, Otitoloju AA. Heavy metal pollution monitoring in vulnerable ecosystems: a case study of the Lagos Lagoon, Nigeria. Bull Environ Contam Toxicol. 2018;100(5):609–13.

    CAS  PubMed  Google Scholar 

  16. Cai F, Calisi RM. Seasons and neighborhoods of high lead toxicity in New York City: the feral pigeon as a bio-indicator. Chemosphere. 2016;161:274–9.

    CAS  PubMed  Google Scholar 

  17. Carrasco KR, Tilbury KL, Myers MS. Assessment of the piscine micronucleus test as an in situ biological indicator of chemical contaminant effects. Can J Fish Aquat Sci. 1990;47:2123–36.

    CAS  Google Scholar 

  18. Carroll RE. The relationship of cadmium in the air to cardiovascular disease rates. J Am Med Assoc. 1966;198:267–9.

    CAS  Google Scholar 

  19. Cavas T, Garanko NN, Arkhipchuk VV. Induction of micronuclei and binuclei in blood, gill and liver cells of fishes subchronically exposed to cadmium chloride and copper sulphate. Food Chem Toxicol. 2005;43:569–74.

    CAS  PubMed  Google Scholar 

  20. Conceicao LEC, Dersjant-Li Y, Verreth JAJ. Cost of growth in larval and juvenile African catfish (Clarias gariepinus) in relation to growth rate, food intake and oxygen consumption. Aquaculture. 1998;161(1–4):95–106.

    Google Scholar 

  21. Crossgrove J, Zheng W. Manganese toxicity upon overexposure. NMR Biomed. 2004;17:544–53.

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Dai W, Liu S, Fu L, Du H, Xu Z. Lead (Pb) accumulation, oxidative stress and DNA damage induced by dietary Pb in tilapia (Oreochromis niloticus). Aquac Res. 2012;43:208–14.

    CAS  Google Scholar 

  23. Das BK, Kaviraj A. Individual and interactive lethal toxicity of cadmium, potassium permanganate and cobalt chloride to fish, worm and plankton. Geobios. 1994;21:223–7.

    CAS  Google Scholar 

  24. Demirak A, Yilmaz F, Tuna AL, Ozdemir N. Heavy metals in water, sediment and tissues of Leuciscus cephalus from a stream in southwestern Turkey. Chemosphere. 2006;63:1451–8.

    CAS  PubMed  Google Scholar 

  25. DeRosa CT, Johnson BL, Fay M, Hansen H, Mumtaz MM. Public health implications of hazardous waste sites: findings, assessment, and research. Food Chem Toxicol. 1996;34:1131–8.

    CAS  Google Scholar 

  26. Dutta TP, Kaviraj A. Acute toxicity of cadmium to fish Labeo rohita and copepod Diaptomus forbesi pre-exposed to CaO and KMnO4. Chemosphere. 2001;42(8):955–8.

    CAS  PubMed  Google Scholar 

  27. EIFAC (European Inland Fisheries Advisory Commission) (1998) Revised report on fish toxicology testing procedures. FAO, Rome. (EIFAC technical paper, no. 24)

  28. Elsokkary IH, Muller G. Assessment and speciation of chromium, nickel, lead and cadmium in the sediments of the River Nile, Egypt. Sci Total Environ. 1990;97(98):455–63.

    Google Scholar 

  29. Fasakin EA, Balogun AM, Ajayi OO. Evaluation of full-fat and defatted maggot meals in the feeding of clariid catfish Clarias gariepinus Fingerlings. Aquac Res. 2003;34:733–8.

    Google Scholar 

  30. Ferraro MVM, Fenocchio AS, Mantovani MS, Ribeiro CDO, Cestari MM. Mutagenic effects of tributyltin and inorganic lead (Pb II) on the fish H. malabaricus as evaluated using the comet assay and the piscine micronucleus and chromosome aberration tests. Genet Mol Biol. 2004;27:103–7.

    CAS  Google Scholar 

  31. Fish JT. Groundwater water treatment for iron and manganese reduction and fish rearing studies applied to the design of the Ruth Burnett Sport Fish Hatchery, Fairbanks, Alaska. Aquac Eng. 2009;41:97–108.

    Google Scholar 

  32. Fulda S, Gorman AM, Hori O, Samali A. Cellular stress responses: cell survival and cell death. Int J Cell Biol. 2010;214074:1–23.

    Google Scholar 

  33. Gabriel D, Riffel APK, Finamor IA, Saccol EMH, Ourique GM, Goulart LO, et al. Effects of sub-chronic manganese chloride exposure on Tambaqui (Colossoma macropomum) tissues: oxidative stress and antioxidant defenses. Arch Environ Contam Toxicol. 2013;64:659–67.

    CAS  PubMed  Google Scholar 

  34. Gil F, Hernández AF, Márquez C, Femia P, Olmedo P, López-Guarnido O, Pla A. Biomonitorization of cadmium, chromium, manganese, nickel and lead in whole blood, urine, axillary hair and saliva in an occupationally exposed population. Sci Total Environ. 2011;409(6):1172–80.

    CAS  PubMed  Google Scholar 

  35. Gisselsson D, Bjork J, Hoglund M, Mertens F, Cin PD, Åkerman M, Mandahl N. Abnormal nuclear shape in solid tumors reflects mitotic instability. Am J Pathol. 2001;158(1):199–206.

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Griffin BR, Davis KB, Darwish A, Straus DL. Effect of exposure to potassium permanganate on stress indicators in channel catfish Ictalurus punctatus. J World Aquac Soc. 2002;33(1):1–9.

    Google Scholar 

  37. Hambach R, Lison D, D’Haese PC, Weyler J, De Graef E, De Schryver A, Lamberts LV, van Sprundel M. Co-exposure to lead increases the renal response to low levels of cadmium in metallurgy workers. Toxicol Lett. 2013;222:233–8.

    CAS  PubMed  Google Scholar 

  38. Howe PD, Malcolm HM, Dobson S (2004) Manganese and its compound: environmental aspects. Concise international chemical assessment document, 63rd edn. World Health Organization, New York

  39. IARC (International Agency for Research on Cancer) (1993) Summaries and evaluations: cadmium and cadmium compounds (group 1). In: IARC monographs on the evaluation of carcinogenic risks to humans, vol 58, Lyon

  40. IARC (International Agency for Research on Cancer) (2006) Inorganic and organic lead compounds. In: IARC monographs on the evaluation of carcinogenic risks to humans, vol 87, Lyon

  41. IPCS (International Programme on Chemical Safety) (1993) Benzene. WHO, Geneva (Environmental Health Criteria, No. 150)

  42. IPCS (International Programme on Chemical Safety) (1992) Cadmium. WHO, Geneva (Environmental Health Criteria, No. 134)

  43. Jarup L. Hazards of heavy metal contamination. Br Med Bull. 2003;68:167–82.

    PubMed  Google Scholar 

  44. Jindal R, Verma S. In vivo genotoxicity and cytotoxicity assessment of cadmium chloride in peripheral erythrocytes of Labeo rohita (Hamilton). Ecotoxicol Environ Saf. 2015;118:1–10.

    CAS  PubMed  Google Scholar 

  45. Katsifis SP, Kinney PL, Hosselet S, Bums FJ, Christie NT. Interaction of nickel with mutagens in the induction of sister chromatid exchanges in human lymphocytes. Mutat Res. 1996;359:7–15.

    PubMed  Google Scholar 

  46. Keen-Kim D, Nooraie F, Nagesh Rao P. Cytogenetic biomarkers for human cancer. Front Biosci. 2008;13:5928–49.

    CAS  PubMed  Google Scholar 

  47. Lambertucci SA, Donázar JA, Huertas AD, Jiménez B, Sáez M, Sanchez-Zapata JA, Hiraldo F. Widening the problem of lead poisoning to a South-American top scavenger: lead concentrations in feathers of wild Andean condors. Biol Conserv. 2011;144:1464–71.

    Google Scholar 

  48. Li Y, Qin J, Wei X, Li C, Wang J, Jiang M, et al. The risk factors of child lead poisoning in China: a meta-analysis. Int J Environ Res Public Health. 2016;13:296–309.

    PubMed Central  Google Scholar 

  49. Lin Y, Ling M, Chen S, Chen W, Hsieh N, Cheng Y, et al. Mixture risk assessment due to ingestion of arsenic, copper, and zinc from milkfish farmed in contaminated coastal areas. Environ Sci Pollut Res. 2017;24:14616–26.

    CAS  Google Scholar 

  50. Liu W, Zhou Q, An J, Sun Y, Liu R. Variations in cadmium accumulation among Chinese cabbage cultivars and screening for Cd-safe cultivars. J Hazard Mater. 2010;173:737–43.

    CAS  PubMed  Google Scholar 

  51. Lo Y, Dooyema CA, Neri A, Durant J, Jefferies T, Medina-Marino A, et al. Childhood lead poisoning associated with gold ore processing: a village-level investigation—Zamfara State, Nigeria, October–November 2010. Environ Health Perspect. 2012;120:1450–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Martinez CBR, Nagae MY, Zaia CTBV, Zaia DAM. Acute morphological and physiological effects of lead in the neotropical fish Prochilodus lineatus. Braz J Biol. 2004;64(4):797–807.

    CAS  PubMed  Google Scholar 

  53. Matsunami J. Hundred years of cadmium poisoning: recollection and prospects, Katsura Shobo, Toyama (2010). In: Kaji M: Role of experts and public participation in pollution control: the case of Itai-itai disease in Japan. Ethics Sci Environ Polit. 2010;12:99–111.

    Google Scholar 

  54. Naigaga I, Kaiser H, Muller WJ, Ojok L, Mbabazi D, Magezi G, Muhumuza E. Fish as bioindicators in aquatic environmental pollution assessment: a case study in Lake Victoria wetlands, Uganda. Phys Chem Earth. 2011;36:918–28.

    Google Scholar 

  55. Nersesyan A, Kundi M, Waldherr M, Setayesh T, Mišík M, Wultsch G, et al. Results of micronucleus assays with individuals who are occupationally and environmentally exposed to mercury, lead and cadmium. Mutat Res. 2016;770:119–39.

    CAS  Google Scholar 

  56. Nriagu JO. Cupellation: the oldest quantitative chemical process. J Chem Educ. 1985;62:668–74.

    CAS  Google Scholar 

  57. Nriagu JO. A silent epidemic of environmental metal poisoning? Environ Pollut. 1988;50:139–61.

    CAS  PubMed  Google Scholar 

  58. Nriagu JO. Global metal pollution: poisoning the biosphere? Environ Sci Policy Sustain Dev. 1990;32(7):7–33.

    Google Scholar 

  59. OECD (Organization for Economic Cooperation and Development) (1992) Guidelines for testing of chemicals. Guideline no. 203: fish, acute toxicity test

  60. O’Neal SL, Zheng W. Manganese toxicity upon overexposure: a decade in review. Curr Environ Health Rep. 2015;2:315–28.

    PubMed  PubMed Central  Google Scholar 

  61. Osman AGM, Abd El Reheen AM, Moustafa MA, Mahmoud UM, Abuel-Fadl KY, Kloas W. In situ evaluation of the genotoxic potential of the river Nile: I. Micronucleus and nuclear lesion tests of erythrocytes of Oreochromis niloticus niloticus (Linnaeus, 1758) and Clarias gariepinus (Burchell, 1822). Toxicol Environ Chem. 2011;93(5):1002–17.

    CAS  Google Scholar 

  62. Özkan F, Gündüz SG, Berköz M, Özlüer Hunt A. Induction of micronuclei and other nuclear abnormalities in peripheral erythrocytes of Nile tilapia, Oreochromis niloticus, following exposure to sublethal cadmium doses. Turk J Zool. 2011;35(4):585–92.

    Google Scholar 

  63. Pal D, Maiti SK. Seasonal variation of heavy metals in water, sediment, and highly consumed cultured fish (Labeo rohita and Labeo bata) and potential health risk assessment in aquaculture pond of the coal city, Dhanbad (India). Environ Sci Pollut Res. 2018;25(13):12464–80.

    CAS  Google Scholar 

  64. Risso-de Faverney C, Devaux A, Lafaurie M, Girard JP, Baillya B, Rahmani R. Cadmium induces apoptosis and genotoxicity in rainbow trout hepatocytes through generation of reactive oxygen species. Aquat Toxicol. 2001;53:65–76.

    CAS  PubMed  Google Scholar 

  65. Romeo M, Mathieu A, Gnassia-Barelli M, Romana A, Lafaurie M. Heavy metal content and biotransformation enzymes in two fish species from the NW Mediterranean. Mar Ecol Prog Ser. 1994;107(1/2):15–22.

    CAS  Google Scholar 

  66. Satarug S, Baker JR, Urbenjapol S, Haswell-Elkins M, Reilly PEB, Williams DJ, et al. A global perspective on cadmium pollution and toxicity in non-occupationally exposed population. Toxicol Lett. 2003;137:65–83.

    CAS  PubMed  Google Scholar 

  67. Schlenk D, Colley WC, El-Alfy A, Kirby R, Griffin BR. Effects of the oxidant potassium permanganate on the expression of gill metallothionein mRNA and its relationship to sublethal whole animal endpoints in channel catfish. Toxicol Sci. 2000;54:177–82.

    CAS  PubMed  Google Scholar 

  68. Sevcikova M, Modra H, Slaninova A, Svobodova Z. Metals as a cause of oxidative stress in fish: a review. Vet Med. 2011;56(11):537–46.

    CAS  Google Scholar 

  69. Shaukat N, Javed M, Ambreen F, Latif F. Oxidative stress biomarker in assessing the lead induced toxicity in commercially important Fish, Labeo rohita. Pak J Zool. 2018;50(2):735–41.

    CAS  Google Scholar 

  70. Shimizu N, Itoh N, Utiyama H, Wahl GM. Selective entrapment of extra-chromosomally amplified DNA by nuclear budding and micronucleation during S phase. J Cell Biol. 1998;140(6):1307–20.

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Singh M. Heavy metal pollution in freshly deposited sediments of the Yamuna river (the Ganges River tibutary): a case study from Delhi and Agra Urban centres, India. Environ Geol (Berlin). 2001;40(6):664–71.

    CAS  Google Scholar 

  72. Slaninova A, Machova J, Svobodova Z. Fish kill caused by aluminium and iron contamination in a natural pond used for fish rearing: a case report. Vet Med. 2014;59(11):573–81.

    CAS  Google Scholar 

  73. Sun H, Li Y, Ji Y, Yang L, Wang W, Li H. Environmental contamination and health hazard of lead and cadmium around Chatian mercury mining deposit in western Hunan Province, China. Trans Nonferr Met Soc China. 2010;20:308–14.

    CAS  Google Scholar 

  74. Taweel A, Shuhaimi-Othman M, Ahmed AK. In vivo acute toxicity tests of some heavy metals to Tilapia fish (Oreochromis niloticus). J Biol Sci. 2013;13(5):365–71.

    CAS  Google Scholar 

  75. Torres C, Creus A, Marcos R. Genotoxic activity of four inhibitors of DNA topoisomerases in larval cells of Drosophila melanogaster as measured in the wing spot assay. Mutat Res. 1998;413:191–203.

    CAS  PubMed  Google Scholar 

  76. Tucker CS, Boyd CE. Relationships between potassium permanganate treatment and water quality. Trans Am Fish Soc. 1977;106:481–8.

    CAS  Google Scholar 

  77. Tuzuki BLL, Delunardo FAC, Ribeiro LN, de Melo CP, Gomes LC, Chippari-Gomes AR. Effects of manganese on fat snook Centropomus parallelusi (Carangaria: Centropomidae) exposed to different temperatures. Neotrop Ichthyol. 2017;15(4):e170054(1–9).

    Google Scholar 

  78. Udroiu I. The micronucleus test in piscine erythrocytes. Aquat Toxicol. 2006;79:201–4.

    CAS  PubMed  Google Scholar 

  79. Verstraeten VL, Peckham LA, Olive M, Capell BC, Collins FS, Nabel EG, et al. Protein farnesylation inhibitors cause donut-shaped cell nuclei attributable to a centrosome separation defect. Proc Natl Acad Sci USA. 2011;108(12):4997–5002.

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Wang D, Du X, Zheng W. Alteration of saliva and serum concentrations of manganese, copper, zinc, cadmium and lead among career welders. Toxicol Lett. 2008;176:40–7.

    CAS  PubMed  Google Scholar 

  81. WHO (World Health Organization) (2003) Benzene in drinking-water. Background document for development of WHO guidelines for drinking-water quality. Geneva. WHO/SDE/WSH/03.04/24; http://www.who.int/water_sanitation_health/dwq/benzene.pdf. Accessed 5 Oct 2016.

  82. WHO (World Health Organization). Environmental health criteria 3: lead. Geneva: World Health Organization; 1977.

    Google Scholar 

  83. Yokel RA. Manganese flux across the blood–brain barrier. NeuroMol Med. 2009;11(4):297–310.

    CAS  Google Scholar 

Download references

Funding

The authors declare that the study herein was not funded by any funding body.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chibuisi G. Alimba.

Ethics declarations

Conflict of interest

The authors declare that no form of conflict of interest exists.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alimba, C.G., Laide, A.W. Genotoxic and cytotoxic assessment of individual and composite mixture of cadmium, lead and manganese in Clarias gariepinus (Burchell 1822) using micronucleus assay. Nucleus 62, 191–202 (2019). https://doi.org/10.1007/s13237-019-00289-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13237-019-00289-w

Keywords

Navigation