Skip to main content

Advertisement

Log in

Antimony-Induced Neurobehavioral and Biochemical Perturbations in Mice

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

Abstract

Groundwater used for drinking has been contaminated with naturally occurring inorganic arsenic and other metals, and metal-contaminated drinking water is the biggest threat to public health in Bangladesh. Toxic metals present in the drinking water have a strong relationship with chronic diseases in humans. Antimony (Sb), a naturally occurring metal, has been reported to be present in the drinking water along with other heavy metals in Bangladesh. Although Sb is present in the environment, very little attention has been given to the toxic effects of Sb. The present study was designed to investigate the in vivo effects of Sb on neurobehavioral changes like anxiety, learning and memory impairment, and blood indices related to organ dysfunction. Mice exposed to antimony potassium-tartrate hydrate (Sb) (10 mg/kg body weight) significantly (p < 0.05) decreased the time spent in open arms while increased the time spent in closed arms compared to the control mice in elevated plus maze. The mean latency time of control group to find the platform decreased (p < 0.05) significantly during 7 days learning as compared to Sb-treated group in Morris water maze test, and Sb-exposed group spent significantly (p < 0.05) less time in the desired quadrant as compared to the control group in probe trial. Sb treatment also significantly altered blood indices related to liver and kidney dysfunction. Additionally, Sb-induced biochemical alterations were associated with significant perturbations in histological architecture of liver and kidney of Sb-exposed mice. These data suggest that Sb has a toxic effect on neurobehavioral and biochemical changes in mice.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Canada)

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  1. Department of Public health engineering, Government of Republic of Bangladesh. Available at http://www.dphe.gov.bd/index.php

  2. EPA (2004) Arsenic in drinking water: treatment technologies, EPA Office of Groundwater and Drinking Water. Available at http://www.epa.gov

  3. Salem HM, Eweida A, Eweida Farag A (2000) Heavy metals in drinking water and their environmental impact on human health. ICEHM 9:542–556

    Google Scholar 

  4. SOS (2014) Arsenic poisoning in Bangladesh. In: The Daily Sun, 2013. Available at http://www.sos-arsenic.net

  5. Chowdhury MAI, Uddin MT, Ahmed MF, Ali MA, Uddin SM (2006) How does arsenic contamination of groundwater causes severity and health hazard in Bangladesh. J Appl Sciences 6:1275–1286

    Article  CAS  Google Scholar 

  6. Tapio S, Grosche B (2006) Arsenic in the aetiology of cancer. Mutation Res 612:215–246

    Article  CAS  Google Scholar 

  7. GuhaMazumder DN, Haque R, Ghosh N, De BK, Santra A, Chakraborty D, Smith AH (1998) Arsenic levels in drinking water and the prevalence of skin lesions in West Bengal, India. Int J Epidemiol 27(5):871–877

    Article  CAS  Google Scholar 

  8. Parvez F, Chen Y, Maria A, Hussain AI, Hassina M, Dhar R, Geen A, Graziano J, Ahsan H (2006) Prevalence of arsenic exposure from drinking water and awareness of its health risks in a Bangladeshi population; results from a large population-based study. Environ Health Perspect 114(3):355–359

    Article  CAS  Google Scholar 

  9. Christina RT, Andrea MA (2014) The effects of arsenic exposure on neurological and cognitive dysfunction in human and rodent studies: a review. Curr Environ Health Rep 1:132–147

    Article  Google Scholar 

  10. Ozone K, Ueno S, Ishizaki M, Hayashi O (2000) Toxicity and oxidative stress induced by organic arsenical diphenylarsinic acid and inorganic arsenicals and their effects on spatial learning ability in mice. J Health Sci 56:517–526

    Article  Google Scholar 

  11. Hei TK, Liu SX, Waldren C (1998) Mutagenicity of arsenic in mammalian cells; role of reactive oxygen species. Proc Natl Acad Sci 95(14):8103–8107

    Article  CAS  Google Scholar 

  12. Liu SX, Athar M, Lippai I, Waldren C, Hei TK (2001) Induction of oxyradicals by arsenic: implication for mechanism of genotoxicity. Proc Natl Acad Sci 98(4):1643–1648

    Article  CAS  Google Scholar 

  13. Frisbie SH, Ortega R, Maynard DM, Sarkar B (2002) The concentrations of arsenic and other toxic elements in Bangladesh’s drinking water. Environ Health Perspect 110(11):1147–1153

    Article  CAS  Google Scholar 

  14. Gebel T (1997) Arsenic and antimony: comparative approach of mechanistic toxicology. Chem Biol Interact 107:131–144

    Article  CAS  Google Scholar 

  15. Gebel T (1999b) Arsenic and drinking water contamination. Science 283:1458–1459

    Article  CAS  Google Scholar 

  16. Gebel T (2000) Confounding variables in the environmental toxicology of arsenic. Toxicology 144:155–162

    Article  CAS  Google Scholar 

  17. McCarty KM, Sen DB, Kile ML, Quamruzzaman K, Rahman M, Mahiuddin G, Christiani DC (2004) Antimony: an unlikely confounder in the relationship between well water arsenic and health outcomes in Bangladesh. Environ Health Persp 112(8):809–812

    Article  CAS  Google Scholar 

  18. Smith KS, Huyck HLO (1999) An overview of the abundance, relative mobility, bioavailability, and human toxicity of metals. In: The environmental geochemistry of mineral deposits, (Plumlee GS, Logsdon MJ, Filipek LH, eds). Reviews in economic geology Vol 6A–B. Littleton, CO: Soc Econ Geologists, 29–70

  19. Ramírez-Campos J, Ramos-Peek J, Martínez-Barros M, Zamora-Peralta M, Martínez-Cerrato J (1998) Peripheral neuropathy caused by acute arsenic poisoning. Gac Med Mex 134(2):241–246

    PubMed  Google Scholar 

  20. Aktar S, Jahan M, Alam S, Mohanto NC, Arefin A, Rahman A, Haque A, Himeno S, Hossain K, Saud ZA (2017) Individual and combined effects of arsenic and lead on behavioral and biochemical changes in mice. Biol Trace Elem Res 177:288–296

    Article  CAS  Google Scholar 

  21. Poon R, Chu I, Lecavaliew P, Vallf VE, Foster E, Gupta S, Thomas B (1998) Effects of antimony on rats following 90-day exposure via drinking water. Food and Chem Toxicol 36:21–35

    Article  CAS  Google Scholar 

  22. Das AP, Bag S, Sahu R, Dua TK, Sinha MK, Gangopadhyay M, Zaman K, Dewanjee S (2010) Protective effect of Corchorus olitorius leaves on sodium arsenite-induced toxicity in experimental rats. Food Chem Toxicol 48:326–335

    Article  CAS  Google Scholar 

  23. Pellow S, Chopin P, File SE, Briley M (1985) Validation of open-closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 14:149–167

    Article  CAS  Google Scholar 

  24. Leret ML, Millan JAS, Antonio MT (2003) Perinatal exposure to lead and cadmium affects anxiety-like behavior. Toxicology 186:125–130

    Article  CAS  Google Scholar 

  25. D'Hooge R, De Deyn PP (2001) Applications of the Morris water maze in the study of learning and memory. Brain Res Brain Res Rev 36(1):60–90

    Article  CAS  Google Scholar 

  26. Noman ASM, Dilruba S, Mohanto NC, Rahman L, Khatun Z, Riad W, Mamun AA, Alam S, Aktar S, Chowdhury S, Saud ZA, Rahman Z, Hossain K (2015) Arsenic-induced histological alterations in various organs of mice. J Cytol Histol 6(3):323

    PubMed  PubMed Central  Google Scholar 

  27. Ali N, Hoque MA, Haque A, Salam KA, Karim MR, Rahman A, Islam K, Saud ZA, Khalek MA, Akhand AA, Hossain M, Mandal A, Karim MR, Miyataka H, Himeno S, Hossain K (2010) Association between arsenic exposure and plasma cholinesterase activity: a population based study in Bangladesh. Environ Health 9:36

    Article  Google Scholar 

  28. Barbier O, Jacquillet G, Tauc M, Cougnon M, Poujeol P (2005) Effect of heavy metals on, and handling by, the kidney. Nephron Physiol 99(4):105–110

    Article  Google Scholar 

  29. Tuot DS, Plantinga LC, Hsu CY, Jordan R, Burrows NR, Hedgeman E, Yee J, Saran R, Powe NR, Centers for Disease Control Chronic Kidney Disease Surveillance Team (2011) Chronic kidney disease awareness among individuals with clinical markers of kidney dysfunction. Clin J Am Soc Nephrol 6(8):1838–1844

    Article  Google Scholar 

  30. Wang JP, Wang SL, Lin Q, Zhang L, Huang D, Nq JC (2009) Association of arsenic and kidney dysfunction in people with diabetes and validation of its effects in rats. Environ Int 35(3):507–511

    Article  CAS  Google Scholar 

  31. McCallum RI (1999) Antimony in medical history. The Pentland Press, Edinburgh

    Google Scholar 

  32. Andra SS, Makris KC, Shine JP, Lu C (2012) Co-leaching of brominated compounds and antimony from bottled water. Environ Int 38:45–53

    Article  CAS  Google Scholar 

  33. Hansen C, Tsirigotaki A, Bak SA, Pergantis SA, Sturup S, Gammelgaard B, Hansen HR (2010) Elevated antimony concentrations in commercial juices. J Environ Monitor 12:822–824

    Article  CAS  Google Scholar 

  34. Gross C, Hen R (2004) The developmental origins of anxiety. Nat Rev Neurosci 5(7):545–552

    Article  CAS  Google Scholar 

  35. Weinberger DR (2001) Anxiety at the frontier of molecular medicine. N Engl J Med 344(16):1247–1249

    Article  CAS  Google Scholar 

  36. Belzung C, Griebel G (2001) Measuring normal and pathological anxiety-like behaviour in mice: a review. Behav Brain Res 125:141–149

    Article  CAS  Google Scholar 

  37. Kahloula K, Slimani M, Aoues A (2009) Behavioural and neurochemical studies of perinatal lead exposed in rat wistar. Eur J Sci Res 35:603–614

    Google Scholar 

  38. Brinkel J, Khan MMH, Kraemer A (2008) A systematic review of arsenic exposure and its social and mental health effects with special reference to Bangladesh. Public Health 6(5):1609–1619

    Google Scholar 

  39. Gandhi DN, Kumar R (2013) Arsenic toxicity and neurobehaviors: a review. Innovat Pharma Pharmacother 1:1–15

    CAS  Google Scholar 

  40. Rahman M, Saud ZA, Hossain E, Islam K, Karim MR, Yeasmin T, Nikkon F, Mandal A, Hossain K (2012) Ameliorating effects of Zingiber zerumbet Linn. on sodium arsenite-induced changes of blood indices in experimental mice. Life Sci Med Res 41

  41. Oyeronke AO, Kazeem AA, Babatunde O, Oladimeji T (2007) Interaction and enhancement of the toxic effects of sodium arsenite and lead acetate in wistar rats. Afr J Biomed Res 10:59–65

    Google Scholar 

  42. Groth DH, Stettler LE, Burg JR, Busey WM, Grant GC, Wong L (1986) Carcinogenic effects of antimony trioxide and antimony ore concentrate in rats. J Toxicol Environ Health 18:607–626

    Article  CAS  Google Scholar 

  43. Newton PE, Bolte HF, Daly IW, Pillsbury BD, Terrill JB, Drew RT, Ben Dyke R, Sheldon AW, Rubin LF (1994) Subchronic and chronic inhalation toxicity of antimony trioxide in the rat. Fundamental Appl Toxicol 22:561–576

    Article  CAS  Google Scholar 

  44. Eisenbach C, Sieg O, Stremmel W, Encke J, Merle U (2007) Diagnostic criteria for acute liver failure due to Wilson disease. World J Gastroenterol 13(11):1711–1714

    Article  Google Scholar 

  45. Kaniaris P, Fassoulaki A, Liarmakopoulou K, Dermitzakis E (1979) Serum cholinesterase levels in patients with cancer. Anesth Analg 58:82–84

    Article  CAS  Google Scholar 

  46. Montenegro MF, Ruiz-Espejo F, Campoy FJ, Muñoz-Delgado E, de la Cadena MP, Cabezas-Herrera J, Vidal CJ (2006) Acetyl- and butyrylcholinesterase activities decrease in human colon adenocarcinoma. J Mol Neurosci 30(1–2):51–54

    Article  CAS  Google Scholar 

  47. Patlolla AK, Tchounwou PB (2005) Serum acetyl cholinesterase as a biomarker of arsenic induced neurotoxicity in Sprague-Dawley rats. Int J Environ Res Public Health 2(1):80–83

    Article  CAS  Google Scholar 

  48. Perrone RD, Madias NE, Levey AS (1992) Serum creatinine as an index of renal function: new insights into old concepts. Clinical Chem 38(10):1933–1953

    CAS  Google Scholar 

  49. Dieter MP, Jameson CW, Elwell MR, Lodge JW, Hejtmancik M, Grumbein SL, Ryan M, Peters AC (1991) Comparative toxicity and tissue distribution of antimony potassium tartrate in rats and mice dosed by drinking water or intraperitoneal injection. J Toxicol Environ Health 34:51–82

    Article  CAS  Google Scholar 

  50. Otto GF, Maren TH, Brown HW (1947) Blood levels and excretion rates of antimony in persons receiving trivalent and pentavalent antimonials. Am J Hygiene 46(2):193–211

    CAS  Google Scholar 

  51. Víctor M, Piñeiro-Carrero E, O Piñeiro (2004) Liver Pediatrics 113(4): 1097–1106

  52. GuhaMazumder DN (2005) Effect of chronic intake of arsenic-contaminated water on liver. Toxicol Appl Pharmacol 206:169–175

    Article  CAS  Google Scholar 

  53. Sarkar S, Mukherjee S, Chattopadhyay A, Bhattacharya S (2014) Low dose of arsenic trioxide triggers oxidative stress in zebrafish brain: expression of antioxidant genes. Ecotoxicol Environ Safety 107:1–8

    Article  CAS  Google Scholar 

  54. Ding X, Su Q, Jiang M, Xie H, Cong J, Wang J (2013) Arsenic affects on cerebellar development of mice. Toxicol Mech Methods 23:672–677

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank MUSC Center for Global Health for their support.

Funding

This work was supported by grants from the University of Rajshahi, Bangladesh (300(6)-5/52/RABI/BINGAN(1) and the grants from the Ministry of Science and Technology, Government of People’s Republic of Bangladesh (39.009.006.01.00.049.2013-2014/BS/104).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zahangir Alam Saud.

Ethics declarations

Ethical approval (No: 67/320/IAMEBBC/IBSC) for this study was taken from the Institutional Animal, Medical Ethics, Biosafety and Biosecurity Committee (IAMEBBC), Institute of Biological Sciences, University of Rajshahi, Bangladesh. All animals received human care in compliance with the institutional guidelines.

Conflict of Interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tanu, T., Anjum, A., Jahan, M. et al. Antimony-Induced Neurobehavioral and Biochemical Perturbations in Mice. Biol Trace Elem Res 186, 199–207 (2018). https://doi.org/10.1007/s12011-018-1290-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-018-1290-5

Keywords

Navigation

-