Advertisement

Neurotoxicity Research

, Volume 36, Issue 4, pp 827–835 | Cite as

Verbal Memory and Learning in Schoolchildren Exposed to Manganese in Mexico

  • Z. García-Chimalpopoca
  • D. Hernández-BonillaEmail author
  • M. Cortez-Lugo
  • C. Escamilla-Núñez
  • A. Schilmann
  • H. Riojas-Rodríguez
  • S. Rodríguez-Dozal
  • S. Montes
  • L. A. Tristán-López
  • M. Catalán-Vázquez
  • C. Rios
Original Article
  • 68 Downloads

Abstract

Manganese (Mn) is an essential nutrient for cellular function, but in high concentrations, it is neurotoxic. Environmental exposure to Mn has been associated with cognitive effects in children. This study aimed to assess the effect of environmental exposure to Mn on verbal memory and learning in schoolchildren residents from two municipalities in the state of Hidalgo, Mexico. Cross-sectional studies were conducted in 2006 and 2013 with a total of 265 schoolchildren of 7 to 11 years old. Children’s Auditory Verbal Learning Test-2 (CAVLT-2) was used to assess verbal memory and learning. Mn exposure tertiles were defined according to hair manganese (MnH) levels determined by atomic absorption spectrophotometry. Linear regression models were used to estimate the association between MnH levels and CAVLT-2 scores. The models were adjusted by potential confounders. The lowest and highest exposure tertiles were defined below and above MnH levels of ≤ 0.72 and ≥ 3.96 μg/g, respectively. Mn exposure was significantly associated with an average of 5- to 9-point decrease in learning curves and summary CAVLT-2 scores in the highest tertile. This study adds to the evidence of decreased verbal memory and learning in schoolchildren environmentally exposed to manganese.

Keywords

Hair manganese Mining area Verbal memory Verbal learning Schoolchildren 

Abbreviations

Mn

Manganese

GABA

Gamma-aminobutyric acid

CNS

Central Nervous System

CAVLT-2

Children’s Auditory Verbal Learning Test-2

MnH

Hair manganese

μg/g

Micrograms per gram

Pb

Lead

PbB

Blood lead

μg/dL

Micrograms per deciliter

Hb

Hemoglobin

g/dL

Grams per deciliter

Notes

Acknowledgments

Our special thanks to all families who participated in this study, and the teachers of the elementary schools “Gral. Ignacio Manuel Altamirano” and “Belisario Dominguez” for all the assistance offered. We thank SJ. Velázquez-Juárez for the design of the study area map. We thank the support of the children’s environmental health Mexico thematic network to publish this paper (CONACyT-Mexico project number 271626).

Funding Sources

This project received funding from the International Development Research Centre (IDRC) project number 100662 and the Consejo Nacional de Ciencia y Tecnología (CONACYT) project number 141385. The funding agencies have not participated in the methodological design of this research.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Bioethics and Research Committees

This study was approved by the Bioethics and Research Committees of the National Institute of Public Health from Mexico.

Informed Consent

Informed consent was obtained from all individual participants included in the study.

References

  1. Afifi AK (2006) Neuroanatomía funcional: texto y atlas. McGraw-Hill, MéxicoGoogle Scholar
  2. Aschner M, Connor JR, Dorman DC et al (2002) In: Massaro EJ (ed) Manganese in health and disease. From transport to neurotoxicity. Handbook of neurotoxicology, vol I. Humana Press Inc, New YorkGoogle Scholar
  3. ATSDR (2007) Agency for toxic substances and disease registry- toxicological profile: lead. http://www.atsdr.cdc.gov/toxprofiles/tp.asp?id=96&tid=22. Accessed 24 Aug 2016
  4. ATSDR (2012) Agency for toxic substances and disease registry- toxicological profile: manganese. http://www.atsdr.cdc.gov/ToxProfiles/TP.asp?id=102&tid=23. Accessed 26 Jan 2015
  5. Bauer JA, Claus Henn B, Austin C et al (2017) Manganese in teeth and neurobehavior: sex-specific windows of susceptibility. Environ Int 108:299–308.  https://doi.org/10.1016/j.envint.2017.08.013 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bouchard M, Laforest F, Vandelac L et al (2007a) Hair manganese and hyperactive behaviors: pilot study of school-age children exposed through tap water. Environ Health Perspect 115:122–127CrossRefGoogle Scholar
  7. Bouchard M, Mergler D, Baldwin M et al (2007b) Neurobehavioral functioning after cessation of manganese exposure: a follow-up after 14 years. Am J Ind Med 50:831–840.  https://doi.org/10.1002/ajim.20407 CrossRefGoogle Scholar
  8. Bouchard M, Sauvé S, Barbeau B, Legrand M et al (2011) Intellectual impairment in school-age children exposed to manganese from drinking water. Environ Health Perspect 119(1):138–143CrossRefGoogle Scholar
  9. Bowman AB, Kwakye GF, Herrero Hernández E, Aschner M (2011) Role of manganese in neurodegenerative diseases. J Trace Elem Med Biol 25:191–203.  https://doi.org/10.1016/j.jtemb.2011.08.144 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Brenneman KA, Wong BA, Buccellato MA et al (2000) Direct olfactory transport of inhaled manganese ((54)MnCl(2)) to the rat brain: toxicokinetic investigations in a unilateral nasal occlusion model. Toxicol Appl Pharmacol 169:238–248.  https://doi.org/10.1006/taap.2000.9073 CrossRefPubMedGoogle Scholar
  11. Caravanos J, Dowling R, Téllez-Rojo MM et al (2014) Blood lead levels in Mexico and pediatric burden of disease implications. Ann Glob Health 80:269–277.  https://doi.org/10.1016/j.aogh.2014.08.002 CrossRefPubMedGoogle Scholar
  12. Carvalho CF, Menezes-Filho JA, de Matos VP et al (2014) Elevated airborne manganese and low executive function in school-aged children in Brazil. Neurotoxicology 45:301–308.  https://doi.org/10.1016/j.neuro.2013.11.006 CrossRefPubMedGoogle Scholar
  13. Carvalho CF, Oulhote Y, Martorelli M et al (2018) Environmental manganese exposure and associations with memory, executive functions, and hyperactivity in Brazilian children. Neurotoxicology 69:253–259.  https://doi.org/10.1016/j.neuro.2018.02.002 CrossRefPubMedGoogle Scholar
  14. CONAPO (2005) Índices de marginación. www.conapo.gob.mx/publicaciones/margina2005 Google Scholar
  15. Dobson AW, Erikson KM, Aschner M (2004) Manganese neurotoxicity. Ann N Y Acad Sci 1012:115–128CrossRefGoogle Scholar
  16. Dorman DC, Brenneman KA, McElveen AM et al (2002) Olfactory transport: a direct route of delivery of inhaled manganese phosphate to the rat brain. J Toxicol Environ Health A 65:1493–1511.  https://doi.org/10.1080/00984100290071630 CrossRefPubMedGoogle Scholar
  17. Elder A, Gelein R, Silva V et al (2006) Translocation of inhaled ultrafine manganese oxide particles to the central nervous system. Environ Health Perspect 114:1172–1178.  https://doi.org/10.1289/ehp.9030 CrossRefPubMedPubMedCentralGoogle Scholar
  18. González-Scarano F, Baltuch G (1999) Microglia as mediators of inflammatory and degenerative diseases. Annu Rev Neurosci 22:219–240.  https://doi.org/10.1146/annurev.neuro.22.1.219 CrossRefPubMedGoogle Scholar
  19. Guilarte TR (2013) Manganese neurotoxicity: new perspectives from behavioral, neuroimaging, and neuropathological studies in humans and non-human primates. Front Aging Neurosci 5:23.  https://doi.org/10.3389/fnagi.2013.00023
  20. Guilarte TR, Chen M-K (2007) Manganese inhibits NMDA receptor channel function: implications to psychiatric and cognitive effects. Neurotoxicology 28:1147–1152.  https://doi.org/10.1016/j.neuro.2007.06.005CrossRefGoogle Scholar
  21. Hernández-Bonilla D, Schilmann A, Montes S et al (2011) Environmental exposure to manganese and motor function of children in Mexico. Neurotoxicology 32:615–621.  https://doi.org/10.1016/j.neuro.2011.07.010 CrossRefPubMedGoogle Scholar
  22. Hernández-Bonilla D, Escamilla-Núñez C, Mergler D et al (2016) Effects of manganese exposure on visuoperception and visual memory in schoolchildren. Neurotoxicology 57:230–240.  https://doi.org/10.1016/j.neuro.2016.10.006 CrossRefPubMedGoogle Scholar
  23. INEGI (2009) Prontuario de información geográfica municipal de los Estados Unidos Mexicanos. Agua Blanca de Iturbide, HidalgoGoogle Scholar
  24. Jiménez MR, Kuhn GR (2009) Toxicología fundamental. Ediciones Díaz de SantosGoogle Scholar
  25. Khan K, Factor-Litvak P, Wasserman GA et al (2011) Manganese exposure from drinking water and children’s classroom behavior in Bangladesh. Environ Health Perspect 119:1501–1506.  https://doi.org/10.1289/ehp.1003397 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Lezak MD, Howieson DB, Bigler ED, Tranel D (2012) Neuropsychological assessment. Oxford University Press, OxfordGoogle Scholar
  27. Lucchini RG, Guazzetti S, Zoni S et al (2012) Tremor, olfactory and motor changes in Italian adolescents exposed to historical ferro-manganese emission. Neurotoxicology 33:687–696.  https://doi.org/10.1016/j.neuro.2012.01.005 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Lussier F, Flessas J (2001) Neuropsychologie de l’Enfant. Troubles Développementaux et de l’Apprentissage. Dunod, FranciaGoogle Scholar
  29. Menezes-Filho JA, Paes CR, Pontes AM et al (2009) High levels of hair manganese in children living in the vicinity of a ferro-manganese alloy production plant. Neurotoxicology 30:1207–1213.  https://doi.org/10.1016/j.neuro.2009.04.005 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Menezes-Filho JA, Novaes C de O, Moreira JC et al (2011) Elevated manganese and cognitive performance in school-aged children and their mothers. Environ Res 111:156–163.  https://doi.org/10.1016/j.envres.2010.09.006 CrossRefPubMedGoogle Scholar
  31. Menezes-Filho JA, de Carvalho-Vivas CF, Viana GFS et al (2014) Elevated manganese exposure and school-aged children’s behavior: a gender-stratified analysis. Neurotoxicology 45:293–300.  https://doi.org/10.1016/j.neuro.2013.09.006 CrossRefPubMedGoogle Scholar
  32. Montes S, Riojas-Rodríguez H, Sabido-Pedraza E, Ríos C (2008) Biomarkers of manganese exposure in a population living close to a mine and mineral processing plant in Mexico. Environ Res 106:89–95.  https://doi.org/10.1016/j.envres.2007.08.008 CrossRefPubMedGoogle Scholar
  33. Moreno JA, Streifel KM, Sullivan KA et al (2009) Developmental exposure to manganese increases adult susceptibility to inflammatory activation of glia and neuronal protein nitration. Toxicol Sci 112:405–415.  https://doi.org/10.1093/toxsci/kfp221 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Oulhote Y, Mergler D, Barbeau B et al (2014a) Neurobehavioral function in school-age children exposed to manganese in drinking water. Environ Health Perspect 122:1343–1350.  https://doi.org/10.1289/ehp.1307918 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Oulhote Y, Mergler D, Bouchard MF (2014b) Sex- and age-differences in blood manganese levels in the U.S. general population: national health and nutrition examination survey 2011-2012. Environ Health 13:87.  https://doi.org/10.1186/1476-069X-13-87 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Raven J (1960) Guide to the standard progressive matrices. HK Lewis, LondresGoogle Scholar
  37. Rice D, Barone S (2000) Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 108:511–533PubMedPubMedCentralGoogle Scholar
  38. Rink SM, Ardoino G, Queirolo EI et al (2014) Associations between hair manganese levels and cognitive, language, and motor development in preschool children from Montevideo, Uruguay. Arch Environ Occup Health 69:46–54.  https://doi.org/10.1080/19338244.2012.725229 CrossRefPubMedGoogle Scholar
  39. Riojas-Rodríguez H, Solís-Vivanco R, Schilmann A et al (2010) Intellectual function in Mexican children living in a mining area and environmentally exposed to manganese. Environ Health Perspect 118:1465–1470CrossRefGoogle Scholar
  40. Rugless F, Bhattacharya A, Succop P et al (2014) Childhood exposure to manganese and postural instability in children living near a ferromanganese refinery in southeastern Ohio. Neurotoxicol Teratol 41:71–79.  https://doi.org/10.1016/j.ntt.2013.12.005 CrossRefPubMedGoogle Scholar
  41. Saputra D, Chang J, Lee B-J et al (2016) Short-term manganese inhalation decreases brain dopamine transporter levels without disrupting motor skills in rats. J Toxicol Sci 41:391–402.  https://doi.org/10.2131/jts.41.391 CrossRefPubMedGoogle Scholar
  42. Saric M, Lucchini R (2007) In: Nordberg GF, Fowler BA, Nordberg M, Friberg L (eds) Manganese. Handbook on the toxicology of metals, 3rd edn. Academic, CambridgeGoogle Scholar
  43. Shin D-W, Kim E-J, Lim S-W et al (2015) Association of hair manganese level with symptoms in attention-deficit/hyperactivity disorder. Psychiatry Investig 12:66–72.  https://doi.org/10.4306/pi.2015.12.1.66 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Talley JL (1997) Children’s Auditory Verbal Learning Test-2 (CAVLT-2). Professional manual. Psychological Assessment Resources, OdessaGoogle Scholar
  45. Torres-Agustín R, Rodríguez-Agudelo Y, Schilmann A et al (2013) Effect of environmental manganese exposure on verbal learning and memory in Mexican children. Environ Res 121:39–44.  https://doi.org/10.1016/j.envres.2012.10.007 CrossRefPubMedGoogle Scholar
  46. Valenzuela M, Oropeza M, Rábago M del R, Solano T (2010) Prevención, diagnóstico y tratamiento de la anemia por deficiencia de hierro en niños y adultos. Guía de Práctica ClínicaGoogle Scholar
  47. Wasserman GA, Liu X, Parvez F et al (2015) Child intelligence and reductions in water arsenic and manganese: a two-year follow-up study in Bangladesh. Environ Health Perspect.  https://doi.org/10.1289/ehp.1509974 CrossRefGoogle Scholar
  48. Weiss B (2000) Vulnerability of children and the developing brain to neurotoxic hazards. Environ Health Perspect 108:375–381PubMedPubMedCentralGoogle Scholar
  49. Winder BS (2010) Manganese in the air: are children at greater risk than adults? J Toxicol Environ Health A 73:156–158.  https://doi.org/10.1080/15287390903340401 CrossRefPubMedGoogle Scholar
  50. Wright RO, Amarasiriwardena C, Woolf AD et al (2006) Neuropsychological correlates of hair arsenic, manganese, and cadmium levels in school-age children residing near a hazardous waste site. Neurotoxicology 27:210–216.  https://doi.org/10.1016/j.neuro.2005.10.001 CrossRefPubMedGoogle Scholar
  51. Zuleta EB (2007) El sistema nervioso : desde las neuronas hasta el cerebro humano. In: Universidad de Antioquia. Medellín, ColombiaGoogle Scholar
  52. Zúñiga FB (1999) Introducción al estudio de la contaminación del suelo por metales pesados. UADY, MéridaGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Z. García-Chimalpopoca
    • 1
  • D. Hernández-Bonilla
    • 1
    Email author
  • M. Cortez-Lugo
    • 1
  • C. Escamilla-Núñez
    • 1
  • A. Schilmann
    • 1
  • H. Riojas-Rodríguez
    • 1
  • S. Rodríguez-Dozal
    • 1
  • S. Montes
    • 2
  • L. A. Tristán-López
    • 2
  • M. Catalán-Vázquez
    • 3
  • C. Rios
    • 2
  1. 1.Environmental Health DepartmentNational Institute of Public HealthCuernavacaMexico
  2. 2.Neurochemistry DepartmentNational Institute of Neurology and NeurosurgeryMexico CityMexico
  3. 3.Clinical Epidemiology DepartmentNational Institute of Respiratory DiseasesMexico CityMexico

Personalised recommendations