Advertisement

Environmental Science and Pollution Research

, Volume 23, Issue 12, pp 12265–12271 | Cite as

Manganese accumulation in hair and teeth as a biomarker of manganese exposure and neurotoxicity in rats

  • Guiqiang Liang
  • Li’e Zhang
  • Shuyan Ma
  • Yingnan Lv
  • Huiyan Qin
  • Xiaowei Huang
  • Li Qing
  • Qin Li
  • Kangcheng Chen
  • Feng Xiong
  • Yifei Ma
  • Jie Nong
  • Xiaobo YangEmail author
  • Yunfeng ZouEmail author
Research Article

Abstract

Manganese (Mn) is an essential trace element to humans. However, excessive Mn causes cognitive impairment resulting from injury to the central nervous system within the hippocampus. No ideal biomarker is currently available for evaluating Mn exposure and associated neurotoxicity in the body. Hence, this study used Mn levels in the serum (MnS), teeth (MnT), and hair (MnH) as biomarkers for evaluating the association between Mn exposure and cognitive impairment in Mn-treated rats. A total of 32 male Sprague–Dawley rats were randomly divided into four groups, received 0, 5, 10, and 20 mg/(kg day) of MnCl2·4H2O for 5 days a week for 18 weeks, respectively. Lifetime Mn cumulative dose (LMCD) was used to evaluate external Mn exposure. Hippocampus, serum, teeth, and hair specimens were collected from the rats for Mn determination by graphite furnace atomic absorption spectrometry. Learning and memory functions were assessed using the Morris water maze test. Results showed that chronic Mn exposure increased the hippocampus (MnHip), MnS, MnT, and MnH levels, as well as impaired learning and memory function in rats. MnHip, MnT, and MnH levels were positively correlated with LMCD (r = 0.759, r = 0.925, and r = 0.908, respectively; p < 0.05), escape latency (r = 0.862, r = 0.716, and r = 0.814, respectively; p < 0.05), and the number of platform crossings (r = −0.734, r = −0.514, and r = −0.566, respectively; p < 0.05). No association was observed between MnS levels and the number of platform crossings (r = −0.286, p > 0.05). Thus, MnT and MnH detected long-term low-dose Mn exposure. These parameters can be reliable biomarkers for Mn exposure and associated neurotoxicity in Mn-treated rats.

Keywords

Rats Manganese neurotoxicity Biomarker Hippocampus Hair Teeth Serum 

Notes

Acknowledgments

This work was financially sponsored by the National Natural Science Foundation of China (Grant Nos. 81160339, 21467003, 81472962, and 21167004), China Postdoctoral Science Foundation (Grant No. 2014M562500XB), Guangxi Natural Science Foundation (Grant No. 2011GXNSFA018187), Scientific Research Foundation of the Education Department of Guangxi Province (Grant No. 201012MS049), and the Guangxi Science Fund for Distinguished Young Scholars (Grant No. 2012GXNSFFA060009).

Compliance with ethical standard

Conflict of interest

The authors declare that they have no conflicts of interest.

References

  1. Apostoli P, Lucchini R Fau - Alessio L, Alessio L (2000) Are current biomarkers suitable for the assessment of manganese exposure in individual workers? Am J Ind Med 37(3)(0271–3586 (Print)):283–290Google Scholar
  2. Arora M, Bradman A, Austin C, Vedar M, Holland N, Eskenazi B, Smith DR (2012) Determining fetal manganese exposure from mantle dentine of deciduous teeth. Environ Sci Technol 46(9):5118–5125CrossRefGoogle Scholar
  3. Aschner M, Guilarte TR, Schneider JS, Zheng W (2007) Manganese: recent advances in understanding its transport and neurotoxicity. Toxicol Appl Pharmacol 221(2):131–147CrossRefGoogle Scholar
  4. Bader M, Dietz Mc Fau - Ihrig A, Ihrig A Fau - Triebig G, Triebig G (1999) Biomonitoring of manganese in blood, urine and axillary hair following low-dose exposure during the manufacture of dry cell batteries. International archives of occupational and environmental health 72(8)(0340–0131 (Print)):521–527Google Scholar
  5. Barton HJ (2011) Advantages of the use of deciduous teeth, hair, and blood analysis for lead and cadmium bio-monitoring in children. A study of 6-year-old children from Krakow (Poland). Biol Trace Elem Res 143(2):637–658CrossRefGoogle Scholar
  6. Blecharz-Klin K, Piechal A, Joniec-Maciejak I, Pyrzanowska J, Widy-Tyszkiewicz E (2012) Effect of intranasal manganese administration on neurotransmission and spatial learning in rats. Toxicol Appl Pharmacol 265(1):1–9CrossRefGoogle Scholar
  7. Eastman RR, Jursa TP, Benedetti C, Lucchini RG, Smith DR (2013) Hair as a biomarker of environmental manganese exposure. Environ Sci Technol 47(3):1629–1637Google Scholar
  8. Fitsanakis VA, Thompson KN, Deery SE, Milatovic D, Shihabi ZK, Erikson KM, Brown RW, Aschner M (2009) A chronic iron-deficient/high-manganese diet in rodents results in increased brain oxidative stress and behavioral deficits in the morris water maze. Neurotox Res 15(2):167–178CrossRefGoogle Scholar
  9. Gunier RB, Bradman A, Jerrett M, Smith DR, Harley KG, Austin C, Vedar M, Arora M, Eskenazi B (2013) Determinants of manganese in prenatal dentin of shed teeth from CHAMACOS children living in an agricultural community. Environ Sci Technol 47(19):11249–11257CrossRefGoogle Scholar
  10. Gunier RB, Arora M, Jerrett M, Bradman A, Harley KG, Mora AM, Koguta K, Hubbarda A, Austinb C, Hollanda N, Eskenazi B (2015) Manganese in teeth and neurodevelopment in young Mexican–American children. Environ Res 142:688–695CrossRefGoogle Scholar
  11. Haynes EN, Heckel P, Ryan P, Roda S, Leung Y-K, Sebastian K, Succop P (2010) Environmental manganese exposure in residents living near a ferromanganese refinery in Southeast Ohio: a pilot study. Neurotoxicology 31(5):468–474CrossRefGoogle Scholar
  12. Hillson S (1996) Dental anthropology: Cambridge University PressGoogle Scholar
  13. Jarvisalo J, Olkinuora M Fau - Kiilunen M, Kiilunen M Fau - Kivisto H, Kivisto H Fau - Ristola P, Ristola P Fau - Tossavainen A, Tossavainen A Fau - Aitio A, Aitio A (1992) Urinary and blood manganese in occupationally nonexposed populations and in manual metal arc welders of mild steel. Int Arch Occup Environ Health. 63(7)(0340–0131 (Print)):495–501Google Scholar
  14. Laohaudomchok W, Lin X, Herrick RF, Fang SC, Cavallari JM, Christiani DC, Weisskopf MG (2011) Toenail, blood, and urine as biomarkers of manganese exposure. J Occup Environ Med 53(5):506–510CrossRefGoogle Scholar
  15. Li X-B, Zhang X, Ju J, Li Y, Yin L, Pu Y (2014) Alterations in neurobehaviors and inflammation in hippocampus of rats induced by oral administration of microcystin-LR. Environ Sci Pollut Res 21(21):12419–12425CrossRefGoogle Scholar
  16. Liang G, Qin H, Zhang L, Ma S, Huang X, Lv Y, Qing L, Li Q, Xiong Y, Huang Y et al (2015) Effects of chronic manganese exposure on the learning and memory of rats by observing the changes in the hippocampal cAMP signaling pathway. Food Chem Toxicol 83:261–267CrossRefGoogle Scholar
  17. Lu L, Zhang L, Li GJ, Guo W, Liang W, Zheng W (2005) Alteration of serum concentrations of manganese, iron, ferritin, and transferrin receptor following exposure to welding fumes among career welders. Neurotoxicology 26(2):257–265CrossRefGoogle Scholar
  18. Menezes-Filho JA, Paes CR, Pontes AM, Moreira JC, Sarcinelli PN, Mergler D (2009) High levels of hair manganese in children living in the vicinity of a ferro-manganese alloy production plant. Neurotoxicology 30(6):1207–1213CrossRefGoogle Scholar
  19. Mora AM, van Wendel de Joode B, Mergler D, Córdoba L, Cano C, Quesada R, Smith DR, Menezes-Filho JA, Lundh T, Lindh CH (2014) Blood and hair Manganese concentrations in pregnant women from the infants’ environmental health study (ISA) in Costa Rica. Environ Sci Technol 48(6):3467–3476CrossRefGoogle Scholar
  20. Mora AM, Arora M, Harley KG, Kogut K, Parra K, Hernández-Bonilla D, Gunier RB, Bradman A, Smith DR, Eskenazi B (2015) Prenatal and postnatal manganese teeth levels and neurodevelopment at 7, 9, and 10.5 years in the CHAMACOS cohort. Environ Int 84:39–54CrossRefGoogle Scholar
  21. Riojas-Rodríguez H, Solís-Vivanco R, Schilmann A, Montes S, Rodríguez S, Ríos C, Rodríguez-Agudelo Y (2010) Intellectual function in Mexican children living in a mining area and environmentally exposed to manganese. Environ Health Perspect 118(10):1465–1470CrossRefGoogle Scholar
  22. Rodríguez-Agudelo Y, Riojas-Rodríguez H, Ríos C, Rosas I, Pedraza ES, Miranda J, Siebe C, Texcalac JL, Santos-Burgoa C (2006) Motor alterations associated with exposure to manganese in the environment in Mexico. Sci Total Environ 368(2):542–556CrossRefGoogle Scholar
  23. Schneider J, Decamp E, Clark K, Bouquio C, Syversen T, Guilarte T (2009) Effects of chronic manganese exposure on working memory in non-human primates. Brain Res 1258:86–95CrossRefGoogle Scholar
  24. Smith D, Gwiazda R, Bowler R, Roels H, Park R, Taicher C, Lucchini R (2007) Biomarkers of Mn exposure in humans. Am J Ind Med 50(11):801–811CrossRefGoogle Scholar
  25. Sriram K, Lin GX, Jefferson AM, Roberts JR, Andrews RN, Kashon ML, Antonini JM (2012) Manganese accumulation in nail clippings as a biomarker of welding fume exposure and neurotoxicity. Toxicology 291(1–3):73–82CrossRefGoogle Scholar
  26. Su C, Chen K, Zou Y, Shen Y, Xia B, Liang G, Lv Y, Wang F, Huang D, Yang X (2015) Chronic exposure to manganese sulfate leads to adverse dose‐dependent effects on the neurobehavioral ability of rats. Environ Toxicol. doi: 10.1002/tox.22161 Google Scholar
  27. Viana GF, de Carvalho CF, Nunes LS, Rodrigues JL, Ribeiro NS, de Almeida DA, Ferreira JR, Abreu N, Menezes-Filho JA (2014) Noninvasive biomarkers of manganese exposure and neuropsychological effects in environmentally exposed adults in Brazil. Toxicol Lett 231(2):169–178CrossRefGoogle Scholar
  28. Wright RO, Amarasiriwardena C, Woolf AD, Jim R, Bellinger DC (2006) Neuropsychological correlates of hair arsenic, manganese, and cadmium levels in school-age children residing near a hazardous waste site. Neurotoxicology 27(2):210–216CrossRefGoogle Scholar
  29. Zheng W, Fu SX, Dydak U, Cowan DM (2011) Biomarkers of manganese intoxication. NeuroToxicology 32(1):1–8CrossRefGoogle Scholar
  30. Zou Y, Qing L, Zeng X, Shen Y, Zhong Y, Liu J, Li Q, Chen K, Lv Y, Huang D et al (2014) Cognitive function and plasma BDNF levels among manganese-exposed smelters. Occup Environ Med 71(3):189–194CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Guiqiang Liang
    • 1
    • 2
  • Li’e Zhang
    • 1
  • Shuyan Ma
    • 1
  • Yingnan Lv
    • 3
  • Huiyan Qin
    • 2
  • Xiaowei Huang
    • 1
  • Li Qing
    • 1
  • Qin Li
    • 1
  • Kangcheng Chen
    • 3
  • Feng Xiong
    • 1
  • Yifei Ma
    • 1
  • Jie Nong
    • 1
  • Xiaobo Yang
    • 3
    Email author
  • Yunfeng Zou
    • 1
    Email author
  1. 1.Teaching and Research Section of Hygienic Toxicology, School of Public HealthGuangxi Medical UniversityNanningPeople’s Republic of China
  2. 2.Institute for Radiation Hygiene Protection, Guangxi Center for Disease Prevention and ControlNanningPeople’s Republic of China
  3. 3.Department of Occupational Health and Environmental Health, School of Public HealthGuangxi Medical UniversityNanningPeople’s Republic of China

Personalised recommendations